Targeted therapies in non-small cell lung cancer: a focus on ALK/ROS1 tyrosine kinase inhibitors

References

• Soda M, Choi YL, Enomoto M, et al. Identification of the transforming EML4–ALK fusion gene in non-small cell lung cancer. Nature. 2007;448:561–566.
   PubMed Web of Science ®Google Scholar
• Camidge DR, Kono SA, Flacco A, et al. Optimizing the detection of lung cancer patients harboring Anaplastic Lymphoma Kinase (ALK) gene rearrangements potentially suitable for ALK inhibitor treatment. Clin Cancer Res. 2010;16:5581–5590.
   PubMed Web of Science ®Google Scholar
• Kwak EL, Bang YJ, Camidge DR, et al. Anaplastic lymphoma kinase inhibition in non–small-cell lung cancer. N Engl J Med. 2010;363:1693–1703.
   PubMed Web of Science ®Google Scholar
• Camidge DR, Bang YJ, Kwak EL, et al. Activity and safety of crizotinib in patients with ALK-positive non-small-cell lung cancer: updated results from a phase 1 study. Lancet Oncol. 2012;13:1011–1019.
   PubMed Web of Science ®Google Scholar
• Kim D-W, Ahn M-J, Shi Y, et al. Results of a global phase II study with crizotinib in advanced ALK-positive non-small cell lung cancer (NSCLC). J Clin Oncol 2012;30:Suppl. abstract 7533.
   Web of Science ®Google Scholar
• Shaw AT, Kim DW, Nakagawa K, et al. Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N Engl J Med. 2013;368:2385–2394.
   PubMed Web of Science ®Google Scholar
• Solomon BJ, Mok T, Kim DW, et al. First-line crizotinib versus chemotherapy in ALK-positive lung cancer. N Engl J Med. 2014;371(23):2167–2177.
   PubMed Web of Science ®Google Scholar
• Gainor JF, Shaw AT. Emerging paradigms in the development of resistance to tyrosine kinase inhibitors in lung cancer. J Clin Oncol. 2013;31(31):3987–3996.
   PubMed Web of Science ®Google Scholar
• Katayama R, Lovly CM, Shaw AT. Therapeutic targeting of anaplastic lymphoma kinase in lung cancer: a paradigm for precision cancer medicine. Clin Cancer Res. 2015;21(10):2227–2235.
   PubMed Web of Science ®Google Scholar
• Shaw AT, Kim DW, Mehra R, et al. Ceritinib in ALK-rearranged non-small-cell lung cancer. N Engl J Med. 2014;370(13):1189–1197.
   PubMed Web of Science ®Google Scholar
• Kim DW, Mehra R, Tan DS, et al. Activity and safety of ceritinib in patients with ALK-rearranged non-small-cell lung cancer (ASCEND-1): updated results from the multicentre, open-label, phase 1 trial. Lancet Oncol. 2016;17(4):452–463.
   PubMed Web of Science ®Google Scholar
• Mok T, Spigel D, Felip E, et al. ASCEND-2: a single-arm, open-label, multicenter phase II study of ceritinib in adult patients (pts) with ALK-rearranged (ALK+) non-small cell lung cancer (NSCLC) previously treated with chemotherapy and crizotinib (CRZ). J Clin Oncol 2015;33:abstr 8059.
   Web of Science ®Google Scholar
• Scagliotti G, Kim TM, Crinò L, et al. Ceritinib versus chemotherapy in patients with advanced ALK+ NSCLC previously treated with chemotherapy and crizotinib: results from the confirmatory phase III ASCEND-5 study. ESMO 2016. Oral presentation. Abstract LBA42.
   Google Scholar
• Felip E, Orlov S, Park K, et al. Phase II study of ceritinib in previously treated ALKi-naïve patients with ALK+ NSCLC: whole-body efficacy in all patients and in patients with baseline brain metastases. ESMO. 2016. Oral 12080.
   Google Scholar
• Felip E, De Brau FG, Maur M, et al. Ceritinib plus nivolumab (NIVO) in patients (pts) with anaplastic lymphoma kinase positive (ALK+) advanced non-small cell lung cancer (NSCLC). J Clin Oncol 2017;35: abstr 2502.
   Web of Science ®Google Scholar
• Soria JC, Tan DS, Chiari R, et al. First-line ceritinib versus platinum-based chemotherapy in advanced ALK-rearranged non-small-cell lung cancer (ASCEND-4): a randomised, open-label, phase 3 study. Lancet. 2017;389(10072):917–929.
   PubMed Web of Science ®Google Scholar
• Kodama T, Hasegawa M, Takanashi K, et al. Anti- tumor activity of the selective ALK inhibi- tor alectinib in models of intracranial metastases. Cancer Chemother Pharmacol. 2014;74:1023–1028.
   PubMed Web of Science ®Google Scholar
• Gadgeel SM, Gandhi L, Riely GJ, et al. Safety and activity of alectinib against systemic disease and brain metastases in patients with crizotinib-resistant ALK- rearranged non-small-cell lung cancer (AF-002JG): results from the dose-finding portion of a phase 1/2 study. Lancet Oncol. 2014;15:1119–1128.
   PubMed Web of Science ®Google Scholar
• Ou SH, Ahn JS, De Petris L, et al. Alectinib in crizotinib-refractory ALK- rearranged non-small-cell lung cancer: a phase II global study. J Clin Oncol. 2016;34:661–668.
   PubMed Web of Science ®Google Scholar
• Seto T, Kiura K, Nishio M, et al. CH5424802 (RO5424802) for patients with ALK-rearranged advanced non-small-cell lung cancer (AF-001JP study): a single-arm, open-label, phase 1–2 study. Lancet Oncol. 2013;14:590–598.
   PubMed Web of Science ®Google Scholar
• Tamura T, Kiura K, Seto T, et al. Three-year follow-up of an alectinib phase I/II study in ALK-positive non–small-cell lung cancer: AF-001JP. J Clin Oncol. 35:1515–1521.
   PubMed Web of Science ®Google Scholar
• Shaw AT, Gandhi L, Gadgeel S, et al. Alectinib in ALK-positive, crizotinib-resistant, non-small-cell lung cancer: a single-group, multicentre, phase 2 trial. Lancet Oncol. 2016;17(2):234–242.
   PubMed Web of Science ®Google Scholar
• Camidge DR, Gadgeel SM, Ou S, et al. Updated efficacy and safety data from the phase 2 NP28761 study of alectinib in ALK-positive non-small-cell lung cancer. Procceding of 17th World Conference on Lung Cancer; Abstract MA07.02.
   Google Scholar
• Gadgeel SM, Shaw AT, Govindan R, et al. Pooled analysis of CNS response to alectinib in two studies of pretreated patients with ALK-positive non-small-cell lung cancer. J Clin Oncol. 2016;34(34):4079–4085.
   PubMed Web of Science ®Google Scholar
• Wolf J, Mazieres J, Oh IJ, et al. Primary results from the phase III ALUR study of alectinib versus chemotherapy in previously treated ALK+ non-small-cell lung cancer (NSCLC). Proceeding of 2017 European Society of Medical Oncology; Madrid, Abstract 1299O_PR.
   Google Scholar
• Hida T, Nokihara H, Kondo M, et al. Alectinib versus crizotinib in patients with ALK-positive non-small-cell lung cancer (J-ALEX): an open-label, randomised phase 3 trial. Lancet. 2017;390(10089):29–39.
   PubMed Web of Science ®Google Scholar
• Takiguchi Y, Hida T, Nokihara H, et al. Updated efficacy and safety of the J-ALEX study comparing alectinib (ALC) with crizotinib (CRZ) in ALK-inhibitor naïve ALK fusion positive non-small cell lung cancer (ALK+ NSCLC). J Clin Oncol 2017;35:abstr 9064.
   Web of Science ®Google Scholar
• Peters S, Camidge DR, Shaw AT, et al. Alectinib versus crizotinib in untreated ALK-positive non-small-cell lung cancer. N Engl J Med. 2017;377(9):829–838.
   PubMed Web of Science ®Google Scholar
• Shaw AT, Peters S, Mok T, et al. Alectinib versus crizotinib in treatment-naive advanced ALK positive Non-Small Cell Lung Cancer (NSCLC): primary results of the global phase III ALEX study. J Clin Oncol 2017;35:(suppl; abstr LBA9008).
   Web of Science ®Google Scholar
• Gadgeel S, Peters S, Mok T, et al. Alectinib vs crizotinib in treatment-naive ALK+ NSCLC: CNS efficacy results from the ALEX study. Proceeding of 2017 European Society of Medical Oncology; Madrid, Abstract 1298O_PR.
   Google Scholar
• Mok T, Peters S, Camidge DR, et al. JCES 01.27 patients with ALK IHC-positive/FISH-negative NSCLC benefit from ALK TKI treatment: response data from the global ALEX trial. J Thorac Oncol. 2017;12(suppl):abstract MA 07.01.
   Google Scholar
• Gettinger SN, Bazhenova LA, Langer CJ, et al. Activity and safety of brigatinib in ALK-rearranged non-small-cell lung cancer and other malignancies: a single-arm, open-label, phase 1/2 trial. The Lancet. 2016;17:1683–1696.
   PubMed Web of Science ®Google Scholar
• Ahn M, Camidge DR, Tiseo M, et al. Brigatinib in crizotinib-refractory ALK+ NSCLC: updated efficacy and safety results from ALTA, a randomized phase 2 trial, Presented at the International Association for the Study of Lung Cancer (IASLC) 18th World Conference on Lung Cancer, OA 05.05. DOI: 10.1016/j.jtho.2017.09.350.
   Google Scholar
• Gainor JF, Dardaei L, Yoda S, et al. Molecular mechanisms of resistance to first- and second-generation ALK inhibitors in ALK-rearranged lung cancer. Cancer Discov. 2016;6:1118–1133.
   PubMed Web of Science ®Google Scholar
• Isozaki H, Ichihara E, Takigawa N, et al. Non-small cell lung cancer cells acquire resistance to the ALK inhibitor alectinib by activating alternative receptor tyrosine kinases. Cancer Res. 2016;76(6):1506–1516.
   PubMed Web of Science ®Google Scholar
• Solomon B, Bauer T, Felip E, et al. Safety and efficacy of lorlatinib (PF- 06463922) from the dose escalation component of a study in patients with advanced ALK+ or ROS1+ non–small cell lung cancer (NSCLC). J Clin Oncol 2016;34:abstr 9009.
   Web of Science ®Google Scholar
• Shaw AT, Ou S-HI, Felip E, et al. Efficacy and safety of lorlatinib in patients (pts) with ALK+ non-small cell lung cancer (NSCLC) with one or more prior ALK tyrosine kinase inhibitor (TKI): a phase I/II study. J Clin Oncol 2017;35:abstr 9006.
   Web of Science ®Google Scholar
• Solomon BJ, Shaw A, Ignatius Ou S-H, et al. Phase 2 Study of lorlatinib in patients with advanced ALK+/ROS1+ non-small-cell lung cancer. Proceeding of the IASLC 18th World Conference on Lung Cancer; 2017 Oct 15–18; Yokohama, Japan. Abstract 8573.
   Google Scholar
• Shaw AT, Friboulet L, Leshchiner I, et al. Resensitization to crizotinib by the lorlatinib ALK resistance mutation L1198F. N Engl J Med. 2016;374:54–61.
   PubMed Web of Science ®Google Scholar
• Gu T-L, Deng X, Huang F, et al. Survey of tyrosine kinase signaling reveals ROS kinase fusions in human cholangiocarcinoma. PLoS One. 2011;6:e15640.
   PubMed Web of Science ®Google Scholar
• Birch AH, Arcand SL, Oros KK, et al. Chromosome 3 anomalies investigated by genome wide SNP analysis of benign, low malignant potential and low grade ovarian serous tumours. PLoS One. 2011;12:e28250.
   Web of Science ®Google Scholar
• Bergethon K, Shaw AT, Ou S-H I, et al. ROS1 rearrangements define a unique molecular class of lung cancers. J Clin Oncol. 2012;30:863–870.
   PubMed Web of Science ®Google Scholar
• Chin LP, Soo RA, Soong R, et al. Targeting ROS1 with anaplastic lymphoma kinase inhibitors. A promising therapeutic strategy for a newly defined molecular subset of non–small-cell lung cancer. J Thorac Oncol. 2012;7:1625–1630.
   PubMed Web of Science ®Google Scholar
• Davies KD, Doebele RC. Molecular pathways: ROS1 fusion proteins in cancer. Clinical Cancer Res. 2013;19:4040–4045.
   PubMed Web of Science ®Google Scholar
• Viola P, Maurya M, Croud J, et al. A validation study for the use of ROS1 immunohistochemical staining in screening for ROS1 translocations in lung cancer. J of Thorac Oncol. 2016;11:1029–1039.
   PubMed Web of Science ®Google Scholar
• Scheffler M, Schultheis A, Teixido C, et al. ROS1 rearrangements in lung adenocarcinoma: prognostic impact, therapeutic options and genetic variability. Oncotarget. 2015;6:10577–10585.
   PubMed Web of Science ®Google Scholar
• Shaw AT, Camidge DR, Engelman JA, et al. Clinical activity of crizotinib in advanced non-small cell lung cancer (NSCLC) harboring ROS1 rearrangement. Presented at the Annual Meeting of the American Society of Clinical Oncology; 2012 Jun 1–5; Chicago. Abstract 7508.
   Google Scholar
• Davies KD, Le AT, Theodoro MF, et al. Identifying and targeting ROS1 gene fusions in non-small cell lung cancer. Clin Cancer Res. 2012;18:4570–4579.
   PubMed Web of Science ®Google Scholar
• Shaw AT, Ou SH, Bang YJ, et al. Crizotinib in ROS1-rearranged non–small-cell lung cancer. N Engl J Med. 2014;371:1963–1971.
   PubMed Web of Science ®Google Scholar
• Mazieres J, Zalcman G, Crinò L, et al. Crizotinib therapy for advanced lung adenocarcinoma and a ROS1 rearrangement: results from the EUROS1 cohort. Clin Oncol. 2015;9:992–999.
   Web of Science ®Google Scholar
• Goto K, Yang JC-H, Kim DW, et al. Phase II study of crizotinib in East Asian patients (pts) with ROS1-positive advanced non-small cell lung cancer (NSCLC). J Clin Oncol. 2016;34:9022.
   Web of Science ®Google Scholar
• Michels S, Gardizi M, Schmalz P, et al. A07.05 EUCROSS: a European phase II trial of crizotinib in advanced adenocarcinoma of the lung harboring ROS1 rearrangements - preliminary results. J Thorac Oncol. 2017;12:S379–S380.
   Web of Science ®Google Scholar
• Moro-Sibilot D, Faivre L, Zalcman G, et al. Crizotinib in patients with advanced ROS1-rearranged non-small cell lung cancer (NSCLC). Preliminary results of the ACSe phase II trial. J Clin Oncol. 2015;33:8065a.
   Web of Science ®Google Scholar
• Awad MM, Katayama R, McTigue M, et al. Acquired resistance to crizotinib from a mutation in CD74-ROS1. N Eng J Med. 2013;368:2395–2401.
   PubMed Web of Science ®Google Scholar
• Katayama R, Kobayashi Y, Friboulet L, et al. Cabozantinib overcomes crizotinib resistance in ROS1 fusion-positive cancer. Clin Cancer Res. 2015;21:166–174.
   PubMed Web of Science ®Google Scholar
• Zou HY, Li Q, Engstrom LD, et al. PF-06463922 is a potent and selective next-generation ROS1/ALK inhibitor capable of blocking crizotinib-resistant ROS1 mutations. Proc Natl Acad Sci USA. 2015;112:3493–3498.
   PubMed Web of Science ®Google Scholar
• Drilon A, Somwar R, Wagne JP, et al. A novel crizotinib-resistant solvent-front mutation responsive to cabozantinib therapy in a patient with ROS1-rearranged lung cancer. Clin Cancer Res. 2015;22:2351–2358.
   PubMed Web of Science ®Google Scholar
• Lim SM, Kim HR, Lee J-S, et al. Open-label, multicenter, phase II study of ceritinib in patients with non–small-cell lung cancer harboring ROS1 rearrangement. Jco 2017. 2017. DOI:10.1200/JCO.2016.71.3701.
   Google Scholar
• Davare MA, Saborowski A, Eide CA, et al. Foretinib is a potent inhibitor of ncogenic ROS1 fusion proteins. Proc Natl Acad Sci USA. 2013;110:19519–19524.
   PubMed Web of Science ®Google Scholar
• Riess JW, Padda SK, Bangs CD, et al. A case series of lengthy progression-free survival with pemetrexed-containing therapy in metastatic non–small-cell lung cancer patients harboring ROS1 gene rearrangements. Clin Lung Cancer. 2013 Sep;14(5):592–595.
   PubMed Web of Science ®Google Scholar
• Chen YF, Hsieh MS, Wu SG, et al. Efficacy of pemetrexed-based chemotherapy in patients with ROS1 fusion-positive lung adenocarcinoma compared with in patients harboring other driver mutations in East Asian populations. J Thorac Oncol. 2016;11:1140–1152.
   PubMed Web of Science ®Google Scholar
• Dziadziuszko R, Le AT, Wrona A, et al. An activating KIT mutation induces crizotinib resistance in ROS1 positive lung cancer. J Thorac Oncol. 2016;11:1273–1281.
   PubMed Web of Science ®Google Scholar
• Davies KD, Mahale S, Astling DP, et al. Resistance to ROS1 inhibition mediated by EGFR pathway activation in non-small cell lung cancer. PLoS One. 2013;8:e82236.
   PubMed Web of Science ®Google Scholar
• Cargnelutti M, Corso S, Pergolizzi M, et al. Activation of RAS family members confers resistance to ROS1 targeting drugs. Oncotarget. 2015;6:5182–5194.
   PubMed Web of Science ®Google Scholar