Hepatocyte growth factor induces gefitinib resistance of lung adenocarcinoma with epidermal growth factor receptor-activating mutations
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Abstract
Lung cancer with epidermal growth factor receptor (EGFR)-activating mutations responds favorably to the EGFR tyrosine kinase inhibitors gefitinib and erlotinib. However, 25% to 30% of patients with EGFR-activating mutations show intrinsic resistance, and the responders invariably acquire resistance to gefitinib. Here, we showed that hepatocyte growth factor (HGF), a ligand of MET oncoprotein, induces gefitinib resistance of lung adenocarcinoma cells with EGFR-activating mutations by restoring the phosphatidylinositol 3-kinase/Akt signaling pathway via phosphorylation of MET, but not EGFR or ErbB3. Strong immunoreactivity for HGF in cancer cells was detected in lung adenocarcinoma patients harboring EGFR-activating mutations, but no T790M mutation or MET amplification, who showed intrinsic or acquired resistance to gefitinib. The findings indicate that HGF-mediated MET activation is a novel mechanism of gefitinib resistance in lung adenocarcinoma with EGFR-activating mutations. Therefore, inhibition of HGF-MET signaling may be a considerable strategy for more successful treatment with gefitinib.
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Activation of MET by its ligand HGF is sufficient to promote resistance through activation of downstream signaling.
“Activation of MET by its ligand hepatic growth factor (HGF) was also sufficient to promote resistance through activation of downstream signaling (Yano et al., 2008).”
From ERBB Receptors: From Oncogene Discovery to Basic Science to Mechanism-Based Cancer Therapeutics (2014) · cites this paper as Yano et al., 2008
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Cites
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., et al. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa040938 · Cited by 11,486 · see citing works
<i>EGFR</i> Mutations in Lung Cancer: Correlation with Clinical Response to Gefitinib Therapy
Paez, J. G., Jänne, P. A., Lee, J. C., Tracy, S., Greulich, H., Gabriel, S., Herman, P., Kaye, F. J., Lindeman, N., Boggon, T. J., et al. (2004) · Science · doi:10.1126/science.1099314 · Cited by 9,368 · see citing works
Comparison of Four Chemotherapy Regimens for Advanced Non–Small-Cell Lung Cancer
Schiller, J. H., Harrington, D., Belani, C. P., Langer, C., Sandler, A., Krook, J., Zhu, J., & Johnson, D. H. (2002) · New England Journal of Medicine · doi:10.1056/nejmoa011954 · Cited by 4,955 · see citing works
<i>MET</i> Amplification Leads to Gefitinib Resistance in Lung Cancer by Activating ERBB3 Signaling
Engelman, J. A., Zejnullahu, K., Mitsudomi, T., Song, Y., Hyland, C., Park, J. O., Lindeman, N., Gale, C.-M., Zhao, X., Christensen, J., et al. (2007) · Science · doi:10.1126/science.1141478 · Cited by 4,496 · see citing works
Self-citation<i>EGFR</i> Mutation and Resistance of Non–Small-Cell Lung Cancer to Gefitinib
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. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa044238 · Cited by 3,964 · see citing works
Pao, W., Miller, V. A., Politi, K. A., Riely, G. J., Somwar, R., Zakowski, M. F., Kris, M. G., & Varmus, H. (2005) · PLoS Medicine · doi:10.1371/journal.pmed.0020073 · Cited by 3,527 · see citing works
ERBB receptors and cancer: the complexity of targeted inhibitors
Hynes, N. E., & Lane, H. A. (2005) · Nature reviews. Cancer · doi:10.1038/nrc1609 · Cited by 3,313 · see citing works
Fukuoka, M., Yano, S., Giaccone, G., Tamura, T., Nakagawa, K., Douillard, J., Nishiwaki, Y., Vansteenkiste, J., Kudoh, S., Rischin, D., et al. (2003) · Journal of Clinical Oncology · doi:10.1200/jco.2003.10.038 · Cited by 2,871 · see citing works
Self-citationMet, metastasis, motility and more
Birchmeier, C., Birchmeier, W., Gherardi, E., & Woude, G. V. (2003) · Nature reviews. Molecular cell biology · doi:10.1038/nrm1261 · Cited by 2,667 · see citing works
Kris, M. G., Natale, R. B., Herbst, R. S., Lynch, Jr., Prager, D., Belani, C. P., Schiller, J. H., Kelly, K., Spiridonidis, H., Sandler, A., et al. (2003) · JAMA · doi:10.1001/jama.290.16.2149 · Cited by 2,517 · see citing works
Stromal fibroblasts in cancer initiation and progression
Bhowmick, N. A., Neilson, E. G., & Moses, H. L. (2004) · Nature · doi:10.1038/nature03096 · Cited by 2,291 · see citing works
Identification of the Hepatocyte Growth Factor Receptor As the c- met Proto-Oncogene Product
Bottaro, D. P., Rubin, J. S., Faletto, D. L., Chan, A. M.-L., Kmiecik, T. E., Woude, G. F. V., & Aaronson, S. A. (1991) · Science · doi:10.1126/science.1846706 · Cited by 2,242 · see citing works
Molecular cloning and expression of human hepatocyte growth factor
Nakamura, T., Nishizawa, T., Hagiya, M., Seki, T., Shimonishi, M., Sugimura, A., Tashiro, K., & Shimizu, S. (1989) · Nature · doi:10.1038/342440a0 · Cited by 2,158 · see citing works
Self-citationBean, J., Brennan, C., Shih, J.-Y., Riely, G., Viale, A., Wang, L., Chitale, D., Motoi, N., Szoke, J., Broderick, S., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710370104 · Cited by 1,598 · see citing works
Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor
Montesano, R., Matsumoto, K., Nakamura, T., & Orci, L. (1991) · Cell · doi:10.1016/0092-8674(91)90363-4 · Cited by 1,147 · see citing works
Self-citationMolecular and chromosomal mechanisms of resistance to imatinib (STI571) therapy
Hochhaus, A., Kreil, S., Corbin, A. S., Rosée, P. G. L., Müller, M., Lahaye, T., Hanfstein, B., Schoch, C., Cross, N. C. P., Berger, U., et al. (2002) · Leukemia · doi:10.1038/sj.leu.2402741 · Cited by 907 · see citing works
Molecular Correlates of Imatinib Resistance in Gastrointestinal Stromal Tumors
Heinrich, M. C., Corless, C. L., Blanke, C. D., Demetri, G. D., Joensuu, H., Roberts, P., Eisenberg, B. L., von Mehren, M., Fletcher, C. D. �., Sandau, K. B., et al. (2006) · Journal of Clinical Oncology · doi:10.1200/jco.2006.06.2265 · Cited by 815 · see citing works
Miller, V. A., Kris, M. G., Shah, N., Patel, J. D., Azzoli, C. G., Gomez, J. E., Krug, L. M., Pao, W. J., Rizvi, N. A., Pizzo, B., et al. (2004) · Journal of Clinical Oncology · doi:10.1200/jco.2004.08.158 · Cited by 729 · see citing works
Naldini, L., Vigna, E., Narsimhan, R. P., Gaudino, G., Zarnegar, R., Michalopoulos, G. K., & Comoglio, P. M. (1991) · PubMed · Cited by 698 · see citing works
Ohe, Y., Ohashi, Y., Kubota, K., Tamura, T., Nakagawa, K., Negoro, S., Nishiwaki, Y., Saijo, N., Ariyoshi, Y., & Fukuoka, M. (2006) · Annals of Oncology · doi:10.1093/annonc/mdl377 · Cited by 633 · see citing works
Mitsudomi, T., & Yatabe, Y. (2007) · Cancer Science · doi:10.1111/j.1349-7006.2007.00607.x · Cited by 606 · see citing works
Self-citationHepatocyte growth factor gene therapy of liver cirrhosis in rats
植木, 孝., Kaneda, Y., Tsutsui, H., Nakanishi, K., Sawa, Y., Morishita, R., Matsumoto, K., Nakamura, T., Takahashi, H., Okamoto, E., et al. (1999) · Nature Medicine · doi:10.1038/5593 · Cited by 588 · see citing works
Self-citationGreen, L. M., Reade, J. L., & Ware, C. F. (1984) · Journal of Immunological Methods · doi:10.1016/0022-1759(84)90190-x · Cited by 560 · see citing works
c-Met as a target for human cancer and characterization of inhibitors for therapeutic intervention
Christensen, J. G., Burrows, J., & Salgia, R. (2004) · Cancer Letters · doi:10.1016/j.canlet.2004.09.044 · Cited by 517 · see citing works
Inoue, A., Suzuki, T., Fukuhara, T., Maemondo, M., Kimura, Y., Morikawa, N., Watanabe, H., Saijo, Y., & Nukiwa, T. (2006) · Journal of Clinical Oncology · doi:10.1200/jco.2005.05.4692 · Cited by 509 · see citing works
Signaling networks assembled by oncogenic EGFR and c-Met
Guo, A., Villén, J., Kornhauser, J. M., Lee, K. A., Stokes, M. P., Rikova, K., Possemato, A. P., Nardone, J., Innocenti, G., Wetzel, R. K., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707270105 · Cited by 502 · see citing works
Dêbiec‐Rychter, M., Cools, J., Dumez, H., Sciot, R., Stul, M. S., Mentens, N., Vranckx, H., Wasąg, B., Prenen, H., Roesel, J. L., et al. (2005) · Gastroenterology · doi:10.1053/j.gastro.2004.11.020 · Cited by 494 · see citing works
Engelman, J. A., Janne, P. A., Mermel, C. H., Pearlberg, J., Mukohara, T., Fleet, C., Cichowski, K. M., Johnson, B. E., & Cantley, L. C. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409773102 · Cited by 494 · see citing works
Lung Cancer Cell Lines Harboring MET Gene Amplification Are Dependent on Met for Growth and Survival
Lutterbach, B. A., Zeng, Q., Davis, L. J., Hatch, H., Hang, G., Kohl, N. E., Gibbs, W. W., & Pan, B. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-3495 · Cited by 321 · see citing works
Morgillo, F., Kim, W.-Y., Kim, E. S., Ciardiello, F., Hong, W. K., & Lee, H. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-2077 · Cited by 249 · see citing works
Hepatocyte growth factor and the Met system as a mediator of tumor–stromal interactions
Matsumoto, K., & Nakamura, T. (2006) · International Journal of Cancer · doi:10.1002/ijc.21808 · Cited by 228 · see citing works
Self-citationIshikawa, N., Daigo, Y., Takano, A., Taniwaki, M., Kato, T., Hayama, S., Murakami, H., Takeshima, Y., Inai, K., Nishimura, H., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-1556 · Cited by 193 · see citing works
Ogino, A., Kitao, H., Hirano, S., Uchida, A., Ishiai, M., Kozuki, T., Takigawa, N., Takata, M., Kiura, K., & Tanimoto, M. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-0681 · Cited by 193 · see citing works
c‐Met activation in lung adenocarcinoma tissues: An immunohistochemical analysis
Nakamura, Y., Niki, T., Goto, A., Morikawa, T., Miyazawa, K., Nakajima, J., & Fukayama, M. (2007) · Cancer Science · doi:10.1111/j.1349-7006.2007.00493.x · Cited by 145 · see citing works
Dual mode regulation of migration by lysophosphatidic acid in human gastric cancer cells
Shida, D., Kitayama, J., Yamaguchi, H., Hama, K., Aoki, J., Arai, H., Yamashita, H., Mori, K., Sako, A., Konishi, T., et al. (2004) · Experimental Cell Research · doi:10.1016/j.yexcr.2004.08.008 · Cited by 71 · see citing works
Chen, J.-T., Lin, T.-S., Chow, K., Huang, H., Chiou, S.-H., Chiang, S., Chen, H., Chuang, T.-L., Lin, T., & Chen, C. (2005) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2005-0117oc · Cited by 54 · see citing works
Wu, W.-J., O'Reilly, M., Langley, R., Tsan, R., Baker, C., Bekele, N., Tang, X.-M., Onn, A., Fidler, I., & Herbst, R. (2007) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-06-0759 · Cited by 50 · see citing works
Kato, S., Funakoshi, H., Nakamura, T., Kato, M., Nakano, I., Hirano, A., & Ohama, E. (2003) · Acta Neuropathologica · doi:10.1007/s00401-003-0708-z · Cited by 44 · see citing works
Self-citationPiacentini, M., Piredda, L., Starace, D., Annicchiarico‐Petruzzelli, M., Mattei, M., Oliverio, S., Farrace, M. G., & Melino, G. (1996) · The Journal of Pathology · doi:10.1002/(sici)1096-9896(199612)180:4 · Cited by 39 · see citing works
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Research works printed but not linked: 1
- Harvey P, Warn A, Newman P, Perry LJ, Ball RY, Warn RM. Immunoreactivity for hepatocyte growth factor/scatter factor and its receptor, met, in human lung carcinomas and malignant mesotheliomas. J Pathol 1996;180:389-94.
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Sequist, L. V., Waltman, B. A., Dias-Santagata, D., Digumarthy, S., Turke, A. B., Fidias, P., Bergethon, K., Shaw, A. T., Gettinger, S., Cosper, A. K., et al. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3002003 · Cited by 3,499 · see citing works
Yu, H. A., Arcila, M. E., Rekhtman, N., Sima, C. S., Zakowski, M. F., Pao, W., Kris, M. G., Miller, V. A., Ladanyi, M., & Riely, G. J. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-2246 · Cited by 2,454 · see citing works
Mechanisms of Acquired Crizotinib Resistance in ALK-Rearranged Lung Cancers
Katayama, R., Shaw, A. T., Khan, T. M., Mino-Kenudson, M. A., Solomon, B., Halmos, B., Jessop, N. A., Wain, J. C., Yeo, A. T., Benes, C. H., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003316 · Cited by 1,316 · see citing works
Rational, biologically based treatment of EGFR-mutant non-small-cell lung cancer
Pao, W., & Chmielecki, J. (2010) · Nature Reviews Cancer · doi:10.1038/nrc2947 · Cited by 1,083 · see citing works
Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC
Turke, A. B., Zejnullahu, K., Wu, Y.-L., Song, Y., Dias-Santagata, D., Lifshits, E., Toschi, L., Rogers, A., Mok, T., Sequist, L., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2009.11.022 · Cited by 1,059 · see citing works
ERBB Receptors: From Oncogene Discovery to Basic Science to Mechanism-Based Cancer Therapeutics
Arteaga, C. L., & Engelman, J. A. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.02.025 · Cited by 1,048 · see citing works
Dissecting Therapeutic Resistance to RAF Inhibition in Melanoma by Tumor Genomic Profiling
Wagle, N., Emery, C., Berger, M. F., Davis, M. J., Sawyer, A. M., Pochanard, P., Kehoe, S. M., Johannessen, C. M., MacConaill, L. E., Hahn, W. C., et al. (2011) · Journal of Clinical Oncology · doi:10.1200/jco.2010.33.2312 · Cited by 996 · see citing works
Mechanisms of acquired resistance to first- and second-generation EGFR tyrosine kinase inhibitors
Westover, D., Zugazagoitia, J., Cho, B. C., Lovly, C. M., & Paz-Ares, L. (2018) · Annals of Oncology · doi:10.1093/annonc/mdx703 · Cited by 766 · see citing works
Understanding resistance to EGFR inhibitors—impact on future treatment strategies
Wheeler, D. L., Dunn, E. F., & Harari, P. M. (2010) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2010.97 · Cited by 683 · see citing works
Lim, Z.-F., & Ma, P. C. (2019) · Journal of Hematology & Oncology · doi:10.1186/s13045-019-0818-2 · Cited by 639 · see citing works
Walter, A. O., Sjin, R. T. T., Haringsma, H. J., Ohashi, K., Sun, J., Lee, K., Dubrovskiy, A., Labenski, M., Zhu, Z., Wang, Z., et al. (2013) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0314 · Cited by 620 · see citing works
Roock, W. D., de Vriendt, V., Normanno, N., Ciardiello, F., & Tejpar, S. (2010) · The Lancet Oncology · doi:10.1016/s1470-2045(10)70209-6 · Cited by 605 · see citing works
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Huang, L., & Fu, L. (2015) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2015.07.001 · Cited by 596 · see citing works
EGFR in Cancer: Signaling Mechanisms, Drugs, and Acquired Resistance
Uribe, M. L., Marrocco, I., & Yarden, Y. (2021) · Cancers · doi:10.3390/cancers13112748 · Cited by 604 · see citing works
Ng, K. P., Hillmer, A. M., Chuah, C. T. H., Juan, W. C., Ko, T. K., Teo, A. S. M., Ariyaratne, P. N., Takahashi, N., Sawada, K., Fei, Y., et al. (2012) · Nature Medicine · doi:10.1038/nm.2713 · Cited by 557 · see citing works
Self-citationNakamura, T., & Mizuno, S. (2010) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.86.588 · Cited by 548 · see citing works
Self-citationCircumventing cancer drug resistance in the era of personalized medicine
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Self-citationEpidermal Growth Factor Receptor Tyrosine Kinase Inhibitor–Resistant Disease
Ohashi, K., Maruvka, Y. E., Michor, F., & Pao, W. (2013) · Journal of Clinical Oncology · doi:10.1200/jco.2012.43.3912 · Cited by 467 · see citing works
Uchibori, K., Inase, N., Araki, M., Kamada, M., Sato, S., Okuno, Y., Fujita, N., & Katayama, R. (2017) · Nature Communications · doi:10.1038/ncomms14768 · Cited by 424 · see citing works
Primrose, J. M., Falk, S. J., Finch-Jones, M., Valle, J. W., O'Reilly, D. A., Siriwardena, A. K., Hornbuckle, J., Peterson, M. C., Rees, M., Iveson, T. J., et al. (2014) · The Lancet Oncology · doi:10.1016/s1470-2045(14)70105-6 · Cited by 425 · see citing works
EGFR-TKIs resistance via EGFR-independent signaling pathways
Liu, Q., Yu, S., Zhao, W., Qin, S., Chu, Q., & Wu, K. (2018) · Molecular Cancer · doi:10.1186/s12943-018-0793-1 · Cited by 413 · see citing works
Treatment approaches for EGFR-inhibitor-resistant patients with non-small-cell lung cancer
Tan, C., Gilligan, D., & Pacey, S. (2015) · The Lancet Oncology · doi:10.1016/s1470-2045(15)00246-6 · Cited by 390 · see citing works
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Mechanisms of resistance to anti-EGFR therapy in colorectal cancer
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Peng, S., Wang, R., Zhang, X., Ma, Y., Zhong, L., Li, K., Nishiyama, A., Arai, S., Yano, S., & Wang, W. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1073-4 · Cited by 314 · see citing works
Self-citationStewart, E., Tan, S. Z., Liu, G., & Tsao, M. (2015) · Europe PMC (PubMed Central) · doi:10.3978/j.issn.2218-6751.2014.11.06 · Cited by 311 · see citing works
Factors underlying sensitivity of cancers to small-molecule kinase inhibitors
Janne, P. A., Gray, N. S., & Settleman, J. (2009) · Nature Reviews Drug Discovery · doi:10.1038/nrd2871 · Cited by 303 · see citing works
Wang, W., Li, Q., Yamada, T., Matsumoto, K., Matsumoto, I., Oda, M., Watanabe, G., Kayano, Y., Nishioka, Y., Sone, S., et al. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-1001 · Cited by 297 · see citing works
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Suda, K., Tomizawa, K., Fujii, M., Murakami, H., Osada, H., Maehara, Y., Yatabe, Y., Sekido, Y., & Mitsudomi, T. (2011) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e318216ee52 · Cited by 277 · see citing works
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Shien, K., Toyooka, S., Yamamoto, H., Soh, J., Jida, M., Thu, K. L., Hashida, S., Maki, Y., Ichihara, E., Asano, H., et al. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-4136 · Cited by 269 · see citing works
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Nagano, T., TACHIHARA, M. Y., & Nishimura, Y. (2018) · Cells · doi:10.3390/cells7110212 · Cited by 252 · see citing works
Yamaguchi, T., Yanagisawa, K., Sugiyama, R., Hosono, Y., Shimada, Y., Arima, C., Kato, S., Tomida, S., Suzuki, M., Osada, H., et al. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.02.008 · Cited by 249 · see citing works
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Hepatocyte growth factor/ MET in cancer progression and biomarker discovery
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Molecular mechanisms of acquired resistance to tyrosine kinase targeted therapy
Sierra, J. R., Cepero, V., & Giordano, S. (2010) · Molecular Cancer · doi:10.1186/1476-4598-9-75 · Cited by 230 · see citing works
Ying, W., Du, Z., Sun, L., Foley, K. P., Proia, D. A., Blackman, R. K., Zhou, D., Inoue, T., Tatsuta, N., Sang, J., et al. (2011) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-11-0755 · Cited by 230 · see citing works
Targeting the HGF/Met signaling pathway in cancer therapy
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Yano, S., Yamada, T., Takeuchi, S., Tachibana, K., Minami, Y., Yatabe, Y., Mitsudomi, T., Tanaka, H., Kimura, T., Kudoh, S., et al. (2011) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e31823ab0dd · Cited by 222 · see citing works
Self-citationQi, J., McTigue, M. A., Rogers, A. M., Lifshits, E., Christensen, J. G., Janne, P. A., & Engelman, J. A. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-1623 · Cited by 218 · see citing works
Cytotoxic Activity of Tivantinib (ARQ 197) Is Not Due Solely to c-MET Inhibition
Katayama, R., Aoyama, A., Yamori, T., Qi, J., Oh‐hara, T., Song, Y., Engelman, J. A., & Fujita, N. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-3256 · Cited by 215 · see citing works
Targeting Receptor Tyrosine Kinase MET in Cancer: Small Molecule Inhibitors and Clinical Progress
Cui, J. J. (2013) · Journal of Medicinal Chemistry · doi:10.1021/jm401427c · Cited by 216 · see citing works
Crosstalk in Met receptor oncogenesis
Lai, A. Z., Abella, J. V., & Park, M. (2009) · Trends in Cell Biology · doi:10.1016/j.tcb.2009.07.002 · Cited by 213 · see citing works
Receptor tyrosine kinases and cancer: oncogenic mechanisms and therapeutic approaches
Saraon, P., Pathmanathan, S., Snider, J. D., Lyakisheva, A., Wong, V., & Štagljar, I. (2021) · Oncogene · doi:10.1038/s41388-021-01841-2 · Cited by 212 · see citing works
Cancer drug-tolerant persister cells: from biological questions to clinical opportunities
Russo, M., Chen, M., Mariella, E., Peng, H., Rehman, S. K., Sancho, E., Sogari, A., Toh, T. S., Balaban, N. Q., Batlle, E., et al. (2024) · Nature Reviews Cancer · doi:10.1038/s41568-024-00737-z · Cited by 210 · see citing works
The Met receptor tyrosine kinase: A key player in oncogenesis and drug resistance
Maroun, C. R., & Rowlands, T. M. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.12.014 · Cited by 207 · see citing works
Terai, H., Soejima, K., Yasuda, H., Nakayama, S., Hamamoto, J., Arai, D., Ishioka, K., Ohgino, K., Ikemura, S., Sato, T., et al. (2013) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-12-0652 · Cited by 207 · see citing works
Suda, K., Murakami, I., Katayama, T., Tomizawa, K., Osada, H., Sekido, Y., Maehara, Y., Yatabe, Y., & Mitsudomi, T. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-1371 · Cited by 204 · see citing works
Self-citationByeon, H. K., Ku, M., & Yang, J. (2019) · Experimental & Molecular Medicine · doi:10.1038/s12276-018-0202-2 · Cited by 199 · see citing works
Cytokines in cancer drug resistance: Cues to new therapeutic strategies
Jones, V. S., Huang, R.-Y., Chen, L.-P., Chen, Z., Fu, L., & Huang, R.-P. (2016) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2016.03.005 · Cited by 196 · see citing works
EGFR-TKI resistance in NSCLC patients: mechanisms and strategies.
Lin, Y., Wang, X., & Jin, H. (2014) · Europe PMC (PubMed Central) · Cited by 198 · see citing works
Emerging roles of deubiquitinases in cancer‐associated pathways
Sacco, J. J., Coulson, J. M., Clague, M. J., & Urbé, S. (2010) · IUBMB Life · doi:10.1002/iub.300 · Cited by 194 · see citing works
Study and analysis of antitumor resistance mechanism of PD1/PD‐L1 immune checkpoint blocker
Wang, Z., & Wu, X. (2020) · Cancer Medicine · doi:10.1002/cam4.3410 · Cited by 200 · see citing works
Benedettini, E., Sholl, L. M., Peyton, M., Reilly, J. F., Ware, C. M., Davis, L. J., Vena, N., Bailey, D., Yeap, B. Y., Fiorentino, M., et al. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090863 · Cited by 187 · see citing works
Mechanisms of drug resistance in kinases
Barouch‐Bentov, R., & Sauer, K. (2011) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.2011.546344 · Cited by 187 · see citing works
The EGFR T790M Mutation in Acquired Resistance to an Irreversible Second-Generation EGFR Inhibitor
Kim, Y.-W., Ko, J., Cui, Z.-Y., Abolhoda, A., Ahn, J. S., Ou, S.-H., Ahn, M., & Park, K. (2012) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-11-0750 · Cited by 179 · see citing works
Lung cancer-associated brain metastasis: Molecular mechanisms and therapeutic options
Yousefi, M., Bahrami, T., Salmaninejad, A., Nosrati, R., Ghaffari, P., & Ghaffari, S. H. (2017) · Cellular Oncology · doi:10.1007/s13402-017-0345-5 · Cited by 177 · see citing works
Hata, A., Katakami, N., Yoshioka, H., Takeshita, J., Tanaka, K., Nanjo, S., Fujita, S., Kaji, R., Imai, Y., Monden, K., et al. (2013) · Cancer · doi:10.1002/cncr.28364 · Cited by 178 · see citing works
HGF Rescues Colorectal Cancer Cells from EGFR Inhibition via MET Activation
Liska, D., Chen, C.-T., Bachleitner-Hofmann, T., Christensen, J. G., & Weiser, M. R. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-0568 · Cited by 176 · see citing works
Epithelial mesenchymal transition in drug resistance and metastasis of lung cancer
Nurwidya, F., Takahashi, F., Murakami, A., & Takahashi, K. (2012) · Cancer Research and Treatment · doi:10.4143/crt.2012.44.3.151 · Cited by 177 · see citing works
Developing c-MET pathway inhibitors for cancer therapy: progress and challenges
Liu, X., Newton, R. C., & Scherle, P. (2009) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2009.11.005 · Cited by 176 · see citing works
Lu, X., Yu, L., Zhang, Z., Ren, X., Smaill, J. B., & Ding, K. (2018) · Medicinal Research Reviews · doi:10.1002/med.21488 · Cited by 173 · see citing works
MET and KRAS Gene Amplification Mediates Acquired Resistance to MET Tyrosine Kinase Inhibitors
Cepero, V., Sierra, J. R., Corso, S., Ghiso, E., Casorzo, L., Perera, T., Comoglio, P. M., & Giordano, S. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-0436 · Cited by 168 · see citing works
Epithelial-mesenchymal transition in EGFR-TKI acquired resistant lung adenocarcinoma.
Uramoto, H., Iwata, T., Onitsuka, T., Shimokawa, H., Hanagiri, T., & Oyama, T. (2010) · PubMed · Cited by 168 · see citing works
Ekert, J. E., Johnson, K., Strake, B., Pardinas, J. R., Jarantow, S. W., Perkinson, R. A., & Colter, D. C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092248 · Cited by 165 · see citing works
Baltschukat, S., Engstler, B. S., Huang, A., Hao, H.-X., Tam, A., Wang, H. Q., Liang, J., DiMare, M. T., Bhang, H.-E. C., Wang, Y., et al. (2019) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-18-2814 · Cited by 163 · see citing works
Cancer Stem Cells—Key Players in Tumor Relapse
Marzagalli, M., Fontana, F., Raimondi, M., & Limonta, P. (2021) · Cancers · doi:10.3390/cancers13030376 · Cited by 135 · see citing works
McDermott, U., Pusapati, R. V., Christensen, J. G., Gray, N. S., & Settleman, J. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-3620 · Cited by 160 · see citing works
Molecular mechanisms of resistance in epidermal growth factor receptor-mutant lung adenocarcinomas
Cortot, A. B., & Jänne, P. A. (2014) · European Respiratory Review · doi:10.1183/09059180.00004614 · Cited by 158 · see citing works
EGFR-TKI Resistance Due to BIM Polymorphism Can Be Circumvented in Combination with HDAC Inhibition
Nakagawa, T., Takeuchi, S., Yamada, T., Ebi, H., Sano, T., Nanjo, S., Ishikawa, D., Sato, M., Hasegawa, Y., Sekido, Y., et al. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-3479 · Cited by 156 · see citing works
Self-citationYamamoto, C., Basaki, Y., Kawahara, A., Nakashima, K., Kage, M., Izumi, H., Kohno, K., Uramoto, H., Yasumoto, K., Kuwano, M., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-0043 · Cited by 155 · see citing works
Hata, A., Katakami, N., Yoshioka, H., Kaji, R., Masago, K., Fujita, S., Imai, Y., Nishiyama, A., Ishida, T., Nishimura, Y., et al. (2015) · Journal of Thoracic Oncology · doi:10.1097/jto.0000000000000647 · Cited by 150 · see citing works
Self-citationArgiris, A. E., Kotsakis, A. P., HOANG, T. N., Worden, F. P., Savvides, P. S., Gibson, M. K., Gyanchandani, R., Blumenschein, G. R., Chen, H. X., Grandis, J. R., et al. (2012) · Annals of Oncology · doi:10.1093/annonc/mds245 · Cited by 148 · see citing works
Yi, Y., Zeng, S., Wang, Z., Wu, M., Ma, Y., Ye, X., Zhang, B., & Liu, H. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.12.021 · Cited by 143 · see citing works
Onitsuka, T., Uramoto, H., Nose, N., Takenoyama, M., Hanagiri, T., Sugio, K., & Yasumoto, K. (2009) · Lung Cancer · doi:10.1016/j.lungcan.2009.05.022 · Cited by 142 · see citing works
Suda, K., Mizuuchi, H., Maehara, Y., & Mitsudomi, T. (2012) · Cancer and Metastasis Reviews · doi:10.1007/s10555-012-9391-7 · Cited by 141 · see citing works
Self-citationKrumbach, R., Schüler, J. B., Hofmann, M., Giesemann, T., Fiebig, H., & Beckers, T. L. (2011) · European Journal of Cancer · doi:10.1016/j.ejca.2010.12.019 · Cited by 141 · see citing works
MiR‐200c inhibits autophagy and enhances radiosensitivity in breast cancer cells by targeting UBQLN1
Sun, Q., Liu, T., Yuan, Y., Guo, Z., Xie, G., Du, S., Lin, X., Xu, Z., Liu, M., Wang, W., et al. (2014) · International Journal of Cancer · doi:10.1002/ijc.29065 · Cited by 140 · see citing works
Self-citationMolecular‐targeted agents combination therapy for cancer: Developments and potentials
Li, F., Zhao, C., & Wang, L. (2013) · International Journal of Cancer · doi:10.1002/ijc.28261 · Cited by 137 · see citing works
Remón, J., Morán, T., Majem, M., Reguart, N., Dalmau, E., Márquez-Medina, D., & LIANES, P. (2013) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2013.06.002 · Cited by 135 · see citing works
Tiedt, R., Degenkolbe, E., Furet, P., Appleton, B. A., Wagner, S., Schoepfer, J. G., Buck, E., Ruddy, D. A., Monahan, J. E., Jones, M. D., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-4433 · Cited by 136 · see citing works
Zou, Y., Ling, Y., Sironi, J., Schwartz, E. L., Perez-Soler, R., & Piperdi, B. (2013) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e31828c7210 · Cited by 134 · see citing works
How Cancer Shapes Evolution and How Evolution Shapes Cancer
Casás‐Selves, M., & DeGregori, J. V. (2011) · Evolution Education and Outreach · doi:10.1007/s12052-011-0373-y · Cited by 134 · see citing works
Karagonlar, Z. F., Koç, D., İşcan, E., Erdal, E., & Atabey, N. (2016) · Cancer Science · doi:10.1111/cas.12891 · Cited by 131 · see citing works
EGFR-mutated oncogene-addicted non-small cell lung cancer: Current trends and future prospects
Soria, J., Mok, T. S. K., Cappuzzo, F., & Janne, P. A. (2011) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2011.10.003 · Cited by 129 · see citing works
Coleman, N., Hong, L., Zhang, J., Heymach, J. V., Hong, D. S., & Le, X. (2021) · ESMO Open · doi:10.1016/j.esmoop.2021.100319 · Cited by 132 · see citing works
Kosaka, T., Yamaki, E., Mogi, A., & Kuwano, H. (2011) · BioMed Research International · doi:10.1155/2011/165214 · Cited by 129 · see citing works
Isozaki, H., Ichihara, E., Takigawa, N., Ohashi, K., Ochi, N., Yasugi, M., Ninomiya, T., Yamane, H., Hotta, K., Sakai, K., et al. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-1010 · Cited by 128 · see citing works
Self-citationBreindel, J. L., Haskins, J. W., Cowell, E. P., Zhao, M., Nguyen, D. X., & Stern, D. F. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-3775 · Cited by 126 · see citing works
Hensing, T. A., Chawla, A., Batra, R., & Salgia, R. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-8778-4_5 · Cited by 125 · see citing works
Acquired resistance to drugs targeting receptor tyrosine kinases
Rosenzweig, S. A. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2011.12.025 · Cited by 122 · see citing works
Liang, H., & Wang, M. (2020) · OncoTargets and Therapy · doi:10.2147/ott.s231257 · Cited by 123 · see citing works
Epidermal Growth Factor Receptor Inhibition in Lung Cancer: Status 2012
Hirsch, F. R., Janne, P. A., Eberhardt, W., Cappuzzo, F., Thatcher, N., Pirker, R., Choy, H., Kim, E. S., Paz-Ares, L. G., Gandara, D. R., et al. (2013) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e31827ed0ff · Cited by 118 · see citing works
Self-citationMolecular Mechanisms and Targeted Therapies Including Immunotherapy for Non-Small Cell Lung Cancer
Nagano, T., TACHIHARA, M. Y., & Nishimura, Y. (2018) · Current Cancer Drug Targets · doi:10.2174/1568009619666181210114559 · Cited by 118 · see citing works
- Authors
- 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.
- Affiliations
- 1Medical Oncology and Divisions of
- Kanazawa University (JP)
- 3Respiratory Medicine and Rheumatology and
- Tokushima University (JP)
- 5Thoracic Surgery and
- Aichi Cancer Center Hospital (JP)
- ORCID
- Venue
- Cancer Research
- Published
- 2008-11-14
- Volume
- 68
- Issue
- 22
- Pages
- 9479-9487
- ISSN
- 0008-5472 (ISSN-L)
- 1538-7445
- OpenAlex
- W2119351872
- Cited by
- 643
- References
- 39
- Citations by year
- 2026: 11 · 2025: 15 · 2024: 11 · 2023: 29 · 2022: 12 · 2021: 33 · 2020: 22 · 2019: 23 · 2018: 43 · 2017: 47 · 2016: 38 · 2015: 52 · 2014: 67 · 2013: 71 · 2012: 58
- FWCI
- 33.79
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- Institutional Repositories DataBase (IRDB) (submittedVersion)
- Kanazawa University Repository for Academic Resources (DSpace) (Kanazawa University) (submittedVersion, cc-by-nc-nd)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Lung Cancer Treatments and Mutations
- Health Sciences › Medicine › Oncology › HER2/EGFR in Cancer Research
- Health Sciences › Medicine › Oncology › Lung Cancer Research Studies
- Keywords
- hepatocyte growth factor, gefitinib resistance, lung adenocarcinoma, EGFR activating mutations, phosphatidylinositol 3-kinase/Akt signaling, EGFR tyrosine kinase inhibitors, HGF/MET signaling, T790M mutation, MET amplification
- MeSH terms
- Gefitinib, Adenocarcinoma, Humans, Lung Neoplasms, Mutation, Phosphorylation, Proto-Oncogene Proteins, Quinazolines, Hepatocyte Growth Factor, Receptors, Growth Factor, Drug Resistance, Neoplasm, Proto-Oncogene Proteins c-met, Phosphatidylinositol 3-Kinases, Receptor, ErbB-3, Cell Line, Tumor, Proto-Oncogene Proteins c-akt, ErbB Receptors
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