Summary of NSCLC EGFR-TKI drugs with the targeted gene mutations and the working mechanisms
Drug(s)
FDA approval specifications and targeted mutations
Generation
Erlotinib, gefitinib, icotinib
Erlotinib: approved in May 2013 for 1st line metastatic and in November 2004 for 2nd line metastatic NSCLC treatment (efficient for exon 19 and L858R mutated NSCLC)
Gefitinib: approved in July 2015 for 1st line metastatic NSCLC. Was earlier approved in 2003 for 3rd line but got retracted in 2005 (diarrhoea and liver dysfunction were noted as adverse effects)
Icotinib was approved in China in June 2011 and caused fewer AEs than gefitinib (61% against 70%), phase III double-blind study revealed a 3–4 months PFS
First
Afatinib, dacominitib
Afatinib got approval in July 2013 for 1st line metastatic, T790M mutant patients & in January 2018 for 1st line metastatic non-resistant mutations
Dacomitinib was approved in September 2018 for 1st line, metastatic NSCLC patients
Second
Osimertinib, rociletinib, olmutinib, lazertinib
Osimertinib was approved by FDA in November 2015 for treating T790M mutated NSCLC besides controlling CNS metastasis
Rociletinib was screened as active in T790M mutated NSCLC in clinical trials but was not approved by FDA due to its limited efficacy
Olmutinib got FDA approval in December 2015 for T790M mutation harboring NSCLC
Lazertinib got its first FDA approval in January 2021 for L858R, exon 19 deleted and T790M mutated advanced, metastasized NSCLC
Third with CNS penetration
1296P BLU-945, MA07.09 BBT-176, BPI-361175
1296P BLU-945 is efficient in treatment of T790M and C797S mutated, advanced NSCLC
MA07.09BBT-176 was manageably toxic for 20–600 mg intake on daily basis, emerging suitable to treat exon 19 deleted, T790M & C797S mutated, advanced NSCLC
BPI-361175 prolonged the life span of exon 19 deleted & T790M/C797S mutated NSCLC in mice models with significant control of CNS metastasis. Currently, it is being evaluated in phase I clinical trials in China & US
Fourth
AEs: adverse events; PFS: progression-free survival; CNS: central nervous system
Declarations
Acknowledgments
The authors would like to thank the School of Chemical Sciences and School of Life Sciences, Central University of Gujarat, ICAR National Research Centre for Equines, Government of India and Amity Institute of Biotechnology for infrastructural and round-the-clock internet facilities.
Author contributions
PM and RR: Conceptualization, Writing—original draft. PM, RR, RS, VHP and TKM: Writing—review & editing. PM and TKM: Validation, Supervision. All authors read and approved the submitted version.
Conflicts of interest
The author declares that there are no conflicts of interest.
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.CA Cancer J Clin. 2018;68:394–424.Erratum in: CA Cancer J Clin. 2020;70:313. [DOI] [PubMed]
Molina JR, Yang P, Cassivi SD, Schild SE, Adjei AA. Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship.Mayo Clin Proc. 2008;83:584–94. [DOI] [PubMed] [PMC]
Korpanty GJ, Graham DM, Vincent MD, Leighl NB. Biomarkers that currently affect clinical practice in lung cancer: EGFR, ALK, MET, ROS-1, and KRAS.Front Oncol. 2014;4:204. [DOI] [PubMed] [PMC]
Lamberti G, Andrini E, Sisi M, Rizzo A, Parisi C, Di Federico A, et al. Beyond EGFR, ALK and ROS1: current evidence and future perspectives on newly targetable oncogenic drivers in lung adenocarcinoma.Crit Rev Oncol Hematol. 2020;156:103119. [DOI] [PubMed]
Oh DY, Fong L. Cytotoxic CD4+ T cells in cancer: expanding the immune effector toolbox.Immunity. 2021;54:2701–11. [DOI] [PubMed] [PMC]
Weigelin B, den Boer AT, Wagena E, Broen K, Dolstra H, de Boer RJ, et al. Cytotoxic T cells are able to efficiently eliminate cancer cells by additive cytotoxicity.Nat Commun. 2021;12:5217. [DOI] [PubMed] [PMC]
Nan X, Xie C, Yu X, Liu J. EGFR TKI as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer.Oncotarget. 2017;8:75712–26. [DOI] [PubMed] [PMC]
Xu L, Xu B, Wang J, Gao Y, He X, Xie T, et al. Recent advances of novel fourth generation EGFR inhibitors in overcoming C797S mutation of lung cancer therapy.Eur J Med Chem. 2023;245:114900. [DOI] [PubMed]
Lim SM, Ahn JS, Hong MH, Kim TM, Jung HA, Ou SH, et al. MA07.09 BBT-176, a 4th generation EGFR TKI, for progressed NSCLC after EGFR TKI therapy: PK, safety and efficacy from phase 1 study.J Thorac Oncol. 2022;17:S70–1. [DOI]
Sequist LV, Lynch TJ. EGFR tyrosine kinase inhibitors in lung cancer: an evolving story.Annu Rev Med. 2008;59:429–42. [DOI] [PubMed]
Berghmans T, Dingemans AM, Hendriks LEL, Cadranel J. Immunotherapy for nonsmall cell lung cancer: a new therapeutic algorithm.Eur Respir J. 2020;55:1901907. [DOI] [PubMed]
Malhotra J, Jabbour SK, Aisner J. Current state of immunotherapy for non-small cell lung cancer.Transl Lung Cancer Res. 2017;6:196–211.Erratum in: Transl Lung Cancer Res. 2017;6:612. [DOI] [PubMed] [PMC]
Shields MD, Marin-Acevedo JA, Pellini B. Immunotherapy for advanced non–small cell lung cancer: a decade of progress.Am Soc Clin Oncol Educ Book. 2021;41:e105–27. [DOI] [PubMed]
Frisone D, Friedlaender A, Addeo A, Tsantoulis P. The landscape of immunotherapy resistance in NSCLC.Front Oncol. 2022;12:817548.Erratum in: Front Oncol. 2023;13:1187021. [DOI] [PubMed] [PMC]
Horvath L, Thienpont B, Zhao L, Wolf D, Pircher A. Overcoming immunotherapy resistance in non-small cell lung cancer (NSCLC) - novel approaches and future outlook.Mol Cancer. 2020;19:141. [DOI] [PubMed] [PMC]
Chaudhary M, Sharma P, Mukherjee TK. Applications of CRISPR/Cas technology against drug-resistant lung cancers: an update.Mol Biol Rep. 2022;49:11491–502. [DOI] [PubMed]
Levantini E, Maroni G, Del Re M, Tenen DG. EGFR signaling pathway as therapeutic target in human cancers.Semin Cancer Biol. 2022;85:253–75. [DOI] [PubMed]
Koulouris A, Tsagkaris C, Corriero AC, Metro G, Mountzios G. Resistance to TKIs in EGFR-mutated non-small cell lung cancer: from mechanisms to new therapeutic strategies.Cancers (Basel). 2022;14:3337. [DOI] [PubMed] [PMC]
Tian X, Gu T, Lee MH, Dong Z. Challenge and countermeasures for EGFR targeted therapy in non-small cell lung cancer.Biochim Biophys Acta Rev Cancer. 2022;1877:188645. [DOI] [PubMed]
Recondo G, Facchinetti F, Olaussen KA, Besse B, Friboulet L. Making the first move in EGFR-driven or ALK-driven NSCLC: first-generation or next-generation TKI?Nat Rev Clin Oncol. 2018;15:694–708. [DOI] [PubMed]
Soria JC, Ohe Y, Vansteenkiste J, Reungwetwattana T, Chewaskulyong B, Lee KH, et al.; FLAURA Investigators. Osimertinib in untreated EGFR-mutated advanced non–small-cell lung cancer.N Engl J Med. 2018;378:113–25. [DOI] [PubMed]
Liang H, Pan Z, Wang W, Guo C, Chen D, Zhang J, et al.; written on behalf of AME Lung Cancer Cooperative Group. The alteration of T790M between 19 del and L858R in NSCLC in the course of EGFR-TKIs therapy: a literature-based pooled analysis.J Thorac Dis. 2018;10:2311–20. [DOI] [PubMed] [PMC]
Qu F, Zhou Y, Yu W. A review of research progress on mechanisms and overcoming strategies of acquired osimertinib resistance.Anticancer Drugs. 2022;33:e76–83. [DOI] [PubMed] [PMC]
Johnson M, Garassino MC, Mok T, Mitsudomi T. Treatment strategies and outcomes for patients with EGFR-mutant non-small cell lung cancer resistant to EGFR tyrosine kinase inhibitors: focus on novel therapies.Lung Cancer. 2022;170:41–51. [DOI] [PubMed]
Tanaka K, Asahina H, Kishimoto J, Miyata Y, Uchida T, Watanabe K, et al. Osimertinib versus osimertinib plus chemotherapy for non–small cell lung cancer with EGFR (T790M)-associated resistance to initial EGFR inhibitor treatment: an open-label, randomised phase 2 clinical trial.Eur J Cancer. 2021;149:14–22. [DOI] [PubMed]
Planchard D, Feng PH, Karaseva N, Kim SW, Kim TM, Lee CK, et al. Osimertinib plus platinum–pemetrexed in newly diagnosed epidermal growth factor receptor mutation-positive advanced/metastatic non-small-cell lung cancer: safety run-in results from the FLAURA2 study.ESMO Open. 2021;6:100271. [DOI] [PubMed] [PMC]
To C, Beyett TS, Jang J, Feng WW, Bahcall M, Haikala HM, et al. An allosteric inhibitor against the therapy-resistant mutant forms of EGFR in non-small cell lung cancer.Nat Cancer. 2022;3:402–17. [DOI] [PubMed] [PMC]
Ahn MJ, Mendoza MJL, Pavlakis N, Kato T, Soo RA, Kim DW, et al. Asian Thoracic Oncology Research Group (ATORG) expert consensus statement on MET alterations in NSCLC: diagnostic and therapeutic considerations.Clin Lung Cancer. 2022;23:670–85. [DOI] [PubMed]
Chan BA, Hughes BG. Targeted therapy for non-small cell lung cancer: current standards and the promise of the future.Transl Lung Cancer Res. 2015;4:36–54. [DOI] [PubMed] [PMC]
Huang L, Fu L. Mechanisms of resistance to EGFR tyrosine kinase inhibitors.Acta Pharm Sin B. 2015;5:390–401. [DOI] [PubMed] [PMC]
van Veggel B, de Langen AJ, Hashemi SMS, Monkhorst K, Heideman DAM, Thunnissen E, et al. Afatinib and cetuximab in four patients with EGFR exon 20 insertion–positive advanced NSCLC.J Thorac Oncol. 2018;13:1222–6. [DOI] [PubMed]
A study of combined C- MET inhibitor and PAN-HER inhibitor (PF-02341066 and PF-00299804) in patients with non- small cell lung cancer [Internet].Source: National Library of Medicine; [cited 2023 Apr 23]. Available from: https://classic.clinicaltrials.gov/ct2/show/NCT01121575
Drilon A, Zhai D, Deng W, Zhang X, Lee D, Rogers E, et al. Abstract 442: Repotrectinib, a next generation TRK inhibitor, overcomes TRK resistance mutations including solvent front, gatekeeper and compound mutations.Cancer Res. 2019;79:442. [DOI]
Drilon A. TRK inhibitors in TRK fusion-positive cancers.Ann Oncol. 2019;30:viii23–30. [DOI] [PubMed] [PMC]
Hirsch FR, Varella-Garcia M, Cappuzzo F. Predictive value of EGFR and HER2 overexpression in advanced non-small-cell lung cancer.Oncogene. 2009;28:S32–7. [DOI] [PubMed]
Pillai RN, Behera M, Berry LD, Rossi MR, Kris MG, Johnson BE, et al. HER2 mutations in lung adenocarcinomas: a report from the lung cancer mutation consortium.Cancer. 2017;123:4099–105. [DOI] [PubMed] [PMC]
Li BT, Shen R, Buonocore D, Olah ZT, Ni A, Ginsberg MS, et al. Ado-trastuzumab emtansine for patients with HER2-mutant lung cancers: results from a phase II basket trial.J Clin Oncol. 2018;36:2532–7.Erratum in: J Clin Oncol. 2019;37:362. [DOI] [PubMed] [PMC]
Lai WV, Lebas L, Barnes TA, Milia J, Ni A, Gautschi O, et al. Afatinib in patients with metastatic or recurrent HER2-mutant lung cancers: a retrospective international multicentre study.Eur J Cancer. 2019;109:28–35. [DOI] [PubMed] [PMC]
Wang Y, Jiang T, Qin Z, Jiang J, Wang Q, Yang S, et al. HER2 exon 20 insertions in non-small-cell lung cancer are sensitive to the irreversible pan-HER receptor tyrosine kinase inhibitor pyrotinib.Ann Oncol. 2019;30:447–55. [DOI] [PubMed] [PMC]
Gao G, Li X, Wang Q, Zhang Y, Chen J, Shu Y, et al. Single-arm, phase II study of pyrotinib in advanced non-small cell lung cancer (NSCLC) patients with HER2 exon 20 mutation.J Cli Oncol. 2019;37:9089. [DOI]
Reita D, Pabst L, Pencreach E, Guérin E, Dano L, Rimelen V, et al. Direct targeting KRAS mutation in non-small cell lung cancer: focus on resistance.Cancers (Basel). 2022;14:1321. [DOI] [PubMed] [PMC]
Lu S, Jang H, Gu S, Zhang J, Nussinov R. Drugging Ras GTPase: a comprehensive mechanistic and signaling structural view.Chem Soc Rev. 2016;45:4929–52. [DOI] [PubMed] [PMC]
Finn SP, Addeo A, Dafni U, Thunnissen E, Bubendorf L, Madsen LB, et al.; European Thoracic Oncology Platform Lungscape Investigators. Prognostic impact of KRAS G12C mutation in patients with NSCLC: results from the European Thoracic Oncology Platform Lungscape Project.J Thorac Oncol. 2021;16:990–1002. [DOI] [PubMed]
Friedlaender A, Drilon A, Weiss GJ, Banna GL, Addeo A. KRAS as a druggable target in NSCLC: rising like a phoenix after decades of development failures.Cancer Treat Rev. 2020;85:101978. [DOI] [PubMed] [PMC]
Hong DS, DuBois SG, Kummar S, Farago AF, Albert CM, Rohrberg KS, et al. Larotrectinib in patients with TRK fusion-positive solid tumours: a pooled analysis of three phase 1/2 clinical trials.Lancet Oncol. 2020;21:531–40. [DOI] [PubMed] [PMC]
Jänne P, Rybkin I, Spira A, Riely G, Papadopoulos K, Sabari J, et al. KRYSTAL-1: activity and safety of adagrasib (MRTX849) in advanced/metastatic non–small-cell lung cancer (NSCLC) harboring KRAS G12C mutation.Eur J Cancer. 2020;138:S1–2. [DOI]
A study to evaluate the safety, pharmacokinetics, and activity of GDC-6036 alone or in combination in participants with advanced or metastatic solid tumors with a KRAS G12C mutation [Internet].Source: National Library of Medicine; [cited 2021 Jan 8]. Available from: https://clinicaltrials.gov/ct2/show/NCT04449874?cond=KRAS+G12C&draw=1&rank=3
Jiao D, Yang S. Overcoming resistance to drugs targeting KRASG12C mutation.Innovation (Camb). 2020;1:100035. [DOI] [PubMed] [PMC]
Kordiak J, Szemraj J, Grabska-Kobylecka I, Bialasiewicz P, Braun M, Kordek R, et al. Intratumor heterogeneity and tissue distribution of KRAS mutation in non-small cell lung cancer: implications for detection of mutated KRAS oncogene in exhaled breath condensate.J Cancer Res Clin Oncol. 2019;145:241–51. [DOI] [PubMed] [PMC]
Xue JY, Zhao Y, Aronowitz J, Mai TT, Vides A, Qeriqi B, et al. Rapid non-uniform adaptation to conformation-specific KRAS(G12C) inhibition.Nature. 2020;577:421–5. [DOI] [PubMed] [PMC]
Brambilla E, Gazdar A. Pathogenesis of lung cancer signalling pathways: roadmap for therapies.Eur Respir J. 2009;33:1485–97. [DOI] [PubMed] [PMC]
Fancelli S, Caliman E, Mazzoni F, Paglialunga L, Gatta Michelet MR, Lavacchi D, et al. KRAS G12 isoforms exert influence over up-front treatments: a retrospective, multicenter, Italian analysis of the impact of first-line immune checkpoint inhibitors in an NSCLC real-life population.Front Oncol. 2022;12:968064. [DOI] [PubMed] [PMC]
Kato S, Fujiwara Y, Hong DS. Targeting KRAS: crossroads of signaling and immune inhibition.J Immunother Precis Oncol. 2022;5:68–78. [DOI] [PubMed] [PMC]
Cullis J, Das S, Bar-Sagi D. Kras and tumor immunity: friend or foe?Cold Spring Harb Perspect Med. 2018;8:a031849. [DOI] [PubMed] [PMC]
Canon J, Rex K, Saiki AY, Mohr C, Cooke K, Bagal D, et al. The clinical KRAS(G12C) inhibitor AMG 510 drives anti-tumour immunity.Nature. 2019;575:217–23. [DOI] [PubMed]
Liu C, Lu H, Wang H, Loo A, Zhang X, Yang G, et al. Combinations with allosteric SHP2 inhibitor TNO155 to block receptor tyrosine kinase signaling.Clin Cancer Res. 2021;27:342–54. [DOI] [PubMed]
Wang X, Allen S, Blake JF, Bowcut V, Briere DM, Calinisan A, et al. Identification of MRTX1133, a noncovalent, potent, and selective KRASG12D inhibitor.J Med Chem. 2022;65:3123–33. [DOI] [PubMed]
Gerlach D, Gmachi M, Ramharter J, Teh J, Fu SC, Trapani F, et al. Abstract 1091: BI-3406 and BI 1701963: potent and selective SOS1::KRAS inhibitors induce regressions in combination with MEK inhibitors or irinotecan.Cancer Res. 2020;80:1091. [DOI]
A study of mRNA-5671/V941 as monotherapy and in combination with pembrolizumab (V941-001) [Internet].Source: National Library of Medicine; [cited 2020 Dec 10]. Available from: https://clinicaltrials.gov/ct2/show/NCT03948763
Kwak EL, Bang YJ, Camidge DR, Shaw AT, Solomon B, Maki RG, et al. Anaplastic lymphoma kinase inhibition in non–small-cell lung cancer.N Engl J Med. 2010;363:1693–703.Erratum in: N Engl J Med. 2011;364:588. [DOI] [PubMed] [PMC]
Gainor JF, Varghese AM, Ou SH, Kabraji S, Awad MM, Katayama R, et al. ALK rearrangements are mutually exclusive with mutations in EGFR or KRAS: an analysis of 1,683 patients with non–small cell lung cancer.Clin Cancer Res. 2013;19:4273–81. [DOI] [PubMed] [PMC]
Morris SW, Kirstein MN, Valentine MB, Dittmer KG, Shapiro DN, Saltman DL, et al. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin’s lymphoma.Science. 1994;263:1281–4.Erratum in: Science. 1995;267:316–7. [DOI] [PubMed]
Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, et al. Identification of the transforming EML4–ALK fusion gene in non-small-cell lung cancer.Nature. 2007;448:561–6. [DOI] [PubMed]
Lazzari C, Spitaleri G, Catania C, Barberis M, Noberasco C, Santarpia M, et al. Targeting ALK in patients with advanced non small cell lung cancer: biology, diagnostic and therapeutic options.Crit Rev Oncol Hematol. 2014;89:358–65. [DOI] [PubMed]
Koivunen JP, Mermel C, Zejnullahu K, Murphy C, Lifshits E, Holmes AJ, et al. EML4-ALK fusion gene and efficacy of an ALK kinase inhibitor in lung cancer.Clin Cancer Res. 2008;14:4275–83. [DOI] [PubMed] [PMC]
Hallberg B, Palmer RH. ALK and NSCLC: targeted therapy with ALK inhibitors.F1000 Med Rep. 2011;3:21. [DOI] [PubMed] [PMC]
Williams AS, Greer W, Bethune D, Craddock KJ, Flowerdew G, Xu Z. ALK+ lung adenocarcinoma in never smokers and long-term ex-smokers: prevalence and detection by immunohistochemistry and fluorescence in situ hybridization.Virchows Arch. 2016;469:533–40. [DOI] [PubMed]
Kim H, Chung JH. Overview of clinicopathologic features of ALK-rearranged lung adenocarcinoma and current diagnostic testing for ALK rearrangement.Transl Lung Cancer Res. 2015;4:149–55. [DOI] [PubMed] [PMC]
Rodig SJ, Mino-Kenudson M, Dacic S, Yeap BY, Shaw A, Barletta JA, et al. Unique clinicopathologic features characterize ALK-rearranged lung adenocarcinoma in the Western population.Clin Cancer Res. 20095;15:5216–23.Erratum in: Clin Cancer Res. 2009;15:7110. [DOI] [PubMed] [PMC]
Solomon BJ, Mok T, Kim DW, Wu YL, Nakagawa K, Mekhail T, et al.; PROFILE 1014 Investigators. First-line crizotinib versus chemotherapy in ALK-positive lung cancer.N Engl J Med. 2014;371:2167–77.Erratum in: N Engl J Med. 2015;373:1582. [DOI] [PubMed]
Kim DW, Mehra R, Tan DSW, Felip E, Chow LQM, Camidge DR, 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;17:452–63. [DOI] [PubMed] [PMC]
Crinò L, Ahn MJ, De Marinis F, Groen HJ, Wakelee H, Hida T, et al. Multicenter phase II study of whole-body and intracranial activity with ceritinib in patients with ALK-rearranged non–small-cell lung cancer previously treated with chemotherapy and crizotinib: results from ASCEND-2.J Clin Oncol. 2016;34:2866–73. [DOI] [PubMed]
Cho BC, Obermannova R, Bearz A, McKeage M, Kim DW, Batra U, et al. Efficacy and safety of ceritinib (450 mg/d or 600 mg/d) with food versus 750-mg/d fasted in patients with ALK receptor tyrosine kinase (ALK)–positive NSCLC: primary efficacy results from the ASCEND-8 study.J Thorac Oncol. 2019;14:1255–65. [DOI] [PubMed]
Soria JC, Tan DSW, Chiari R, Wu YL, Paz-Ares L, Wolf J, 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;389:917–29.Erratum in: Lancet. 2017;389:908. [DOI] [PubMed]
Shaw AT, Kim TM, Crinò L, Gridelli C, Kiura K, Liu G, et al. Ceritinib versus chemotherapy in patients with ALK-rearranged non-small-cell lung cancer previously given chemotherapy and crizotinib (ASCEND-5): a randomised, controlled, open-label, phase 3 trial.Lancet Oncol. 2017;18:874–86. [DOI] [PubMed]
Peters S, Camidge DR, Shaw AT, Gadgeel S, Ahn JS, Kim DW, et al.; ALEX Trial Investigators. Alectinib versus crizotinib in untreated ALK-positive non–small-cell lung cancer.N Engl J Med. 2017;377:829–38. [DOI] [PubMed]
Camidge DR, Peters S, Mok T, Gadgeel SM, Cheema PK, Pavlakis N, et al. Updated efficacy and safety data from the global phase III ALEX study of alectinib (ALC) vs crizotinib (CZ) in untreated advanced ALK+ NSCLC.J Clin Oncol. 2018;36:9043. [DOI]
Camidge DR, Kim HR, Ahn MJ, Yang JC, Han JY, Lee JS, et al. Brigatinib versus crizotinib in ALK-positive non–small-cell lung cancer.N Engl J Med. 2018;379:2027–39. [DOI] [PubMed]
Camidge DR, Kim HR, Ahn MJ, Yang JCH, Han JY, Hochmair MJ, et al. Brigatinib versus crizotinib in ALK inhibitor–naive advanced ALK-positive NSCLC: final results of phase 3 ALTA-1L trial.J Thorac Oncol. 2021;16:2091–108.Erratum in: J Thorac Oncol. 2022;[Epub ahead of print]. [DOI] [PubMed]
Stinchcombe TE, Doebele RC, Wang X, Gerber DE, Horn L, Camidge DR. Preliminary clinical and molecular analysis results from a single-arm phase 2 trial of brigatinib in patients with disease progression after next-generation ALK tyrosine kinase inhibitors in advanced ALK+ NSCLC.J Thorac Oncol. 2021;16:156–61. [DOI] [PubMed]
Popat S, Liu G, Lu S, Song G, Ma X, Yang JC. Brigatinib vs alectinib in crizotinib-resistant advanced anaplastic lymphoma kinase-positive non-small-cell lung cancer (ALTA-3).Future Oncol. 2021;17:4237–47. [DOI] [PubMed]
Peng L, Zhu L, Sun Y, Stebbing J, Selvaggi G, Zhang Y, et al. Targeting ALK rearrangements in NSCLC: current state of the art.Front Oncol. 2022;12:863461. [DOI] [PubMed] [PMC]
Horn L, Infante JR, Reckamp KL, Blumenschein GR, Leal TA, Waqar SN, et al. Ensartinib (X-396) in ALK-positive non–small cell lung cancer: results from a first-in-human phase I/II, multicenter study.Clin Cancer Res. 2018;24:2771–9. [DOI] [PubMed] [PMC]
Horn L, Wu YL, Reck M, Wakelee HA, Liang C, Tan F, et al. eXalt3: phase 3 randomized study comparing ensartinib to crizotinib in anaplastic lymphoma kinase (ALK) positive non-small cell lung cancer (NSCLC) patients.J Clin Oncol. 2018;36:TPS9115. [DOI]
Basit S, Ashraf Z, Lee K, Latif M. First macrocyclic 3rd-generation ALK inhibitor for treatment of ALK/ROS1 cancer: clinical and designing strategy update of lorlatinib.Eur J Med Chem. 2017;134:348–56. [DOI] [PubMed]
Solomon BJ, Besse B, Bauer TM, Felip E, Soo RA, Camidge DR, et al. Lorlatinib in patients with ALK-positive non-small-cell lung cancer: results from a global phase 2 study.Lancet Oncol. 2018;19:1654–67. [DOI] [PubMed]
Shaw AT, Bauer TM, de Marinis F, Felip E, Goto Y, Liu G, et al.; CROWN Trial Investigators. First-line lorlatinib or crizotinib in advanced ALK-positive lung cancer.N Engl J Med. 2020;383:2018–29. [DOI] [PubMed]
Murray BW, Zhai D, Deng W, Zhang X, Ung J, Nguyen V, et al. TPX-0131, a potent CNS-penetrant, next-generation inhibitor of wild-type ALK and ALK-resistant mutations.Mol Cancer Ther. 2021;20:1499–507. [DOI] [PubMed] [PMC]
Pelish HE, Tangpeerachaikul A, Kohl NE, Porter JR, Shair MD, Horan JC. Abstract 1468: NUV-655 (NVL-655) is a selective, brain-penetrant ALK inhibitor with antitumor activity against the lorlatinib-resistant G1202R/L1196M compound mutation.Cancer Res. 2021;81:1468. [DOI]
Ardini E, Menichincheri M, Banfi P, Bosotti R, De Ponti C, Pulci R, et al. Entrectinib, a pan–TRK, ROS1, and ALK inhibitor with activity in multiple molecularly defined cancer indications.Mol Cancer Ther. 2016;15:628–39. [DOI] [PubMed]
Drilon A, Ou SH, Cho BC, Kim DW, Lee J, Lin JJ, et al. Repotrectinib (TPX-0005) is a next-generation ROS1/TRK/ALK inhibitor that potently inhibits ROS1/TRK/ALK solvent- front mutations.Cancer Discov. 2018;8:1227–36. [DOI] [PubMed]
Drilon A, Siena S, Ou SI, Patel M, Ahn MJ, Lee J, et al. Safety and antitumor activity of the multitargeted pan-TRK, ROS1, and ALK inhibitor entrectinib: combined results from two phase I trials (ALKA-372-001 and STARTRK-1).Cancer Discov. 2017;7:400–9. [DOI] [PubMed] [PMC]
Cho BC, Drilon AE, Doebele RC, Kim DW, Lin JJ, Lee J, et al. Safety and preliminary clinical activity of repotrectinib in patients with advanced ROS1 fusion-positive non-small cell lung cancer (TRIDENT-1 study).J Clin Oncol. 2019;37:9011. [DOI]
Costa DB, Kobayashi S, Pandya SS, Yeo WL, Shen Z, Tan W, et al. CSF concentration of the anaplastic lymphoma kinase inhibitor crizotinib.J Clin Oncol. 2011;29:e443–5. [DOI] [PubMed]
Choi YL, Soda M, Yamashita Y, Ueno T, Takashima J, Nakajima T, et al.; ALK Lung Cancer Study Group. EML4-ALK mutations in lung cancer that confer resistance to ALK inhibitors.N Engl J Med. 2010;363:1734–9. [DOI] [PubMed]
Yanagitani N, Uchibori K, Koike S, Tsukahara M, Kitazono S, Yoshizawa T, et al. Drug resistance mechanisms in Japanese anaplastic lymphoma kinase-positive non–small cell lung cancer and the clinical responses based on the resistant mechanisms.Cancer Sci. 2020;111:932–9. [DOI] [PubMed] [PMC]
Ando K, Manabe R, Kishino Y, Kusumoto S, Yamaoka T, Tanaka A, et al. Comparative efficacy and safety of lorlatinib and alectinib for ALK-rearrangement positive advanced non-small cell lung cancer in Asian and non-Asian patients: a systematic review and network meta-analysis.Cancers (Basel). 2021;13:3704. [DOI] [PubMed] [PMC]
Ma Y, Yang N, Li S, Zhao H, Li L, Yang H, et al. A phase I, dose-escalation and expansion study of TQ-B3139, a novel ALK TKI, in Chinese ALK or ROS1 positive advanced non-small cell lung cancer (NSCLC).J Clin Oncol. 2020;38:9585. [DOI]
Shi Y, Fang J, Hao X, Zhang S, Liu Y, Wang L, et al. Safety and activity of WX-0593 (iruplinalkib) in patients with ALK- or ROS1-rearranged advanced non-small cell lung cancer: a phase 1 dose-escalation and dose-expansion trial.Signal Transduct Target Ther. 2022;7:25. [DOI] [PubMed] [PMC]
Han B, Chu T, Qian J, Yan B, Zhang Y, Chang Q. P2.01-31 Preliminary results of second generation ALK inhibitor PLB1003: a phase la study.J Thorac Oncol. 2019;14:S651. [DOI]
Xia ZJ, Ji YC, Sun DQ, Peng X, Gao YL, Fang YF, et al. SAF-189s, a potent new-generation ROS1 inhibitor, is active against crizotinib-resistant ROS1 mutant-driven tumors.Acta Pharmacol Sin. 2021;42:998–1004. [DOI] [PubMed] [PMC]
Song P, Zhang X, Yang D, Wang H, Si X, Zhang L. Single-center study to determine the safety and efficacy of CT-707 in Chinese patients with advanced anaplastic lymphoma kinase-rearranged non-small-cell lung cancer.Thorac Cancer. 2020;11:1216–23. [DOI] [PubMed] [PMC]
Powell CE, Gao Y, Tan L, Donovan KA, Nowak RP, Loehr A, et al. Chemically induced degradation of anaplastic lymphoma kinase (ALK).J Med Chem. 2018;61:4249–55. [DOI] [PubMed] [PMC]
Wang Y, Han L, Liu F, Yang F, Jiang X, Sun H, et al. Targeted degradation of anaplastic lymphoma kinase by gold nanoparticle-based multi-headed proteolysis targeting chimeras.Colloids Surf B Biointerfaces. 2020;188:110795. [DOI] [PubMed]
Sun N, Ren C, Kong Y, Zhong H, Chen J, Li Y, et al. Development of a brigatinib degrader (SIAIS117) as a potential treatment for ALK positive cancer resistance.Eur J Med Chem. 2020;193:112190. [DOI] [PubMed]
Song X, Zhong H, Qu X, Yang L, Jiang B. Two novel strategies to overcome the resistance to ALK tyrosine kinase inhibitor drugs: macrocyclic inhibitors and proteolysis-targeting chimeras.MedComm (2020). 2021;2:341–50. [DOI] [PubMed] [PMC]
Shaw AT, Riely GJ, Bang YJ, Kim DW, Camidge DR, Solomon BJ, et al. Crizotinib in ROS1-rearranged advanced non-small-cell lung cancer (NSCLC): updated results, including overall survival, from PROFILE 1001.Ann Oncol. 2019;30:1121–6. [DOI] [PubMed] [PMC]
Moro-Sibilot D, Faivre L, Zalcman G, Pérol M, Barlesi F, Monnet JO. Crizotinib in patients with advanced ROS1-rearranged non-small cell lung cancer (NSCLC). Preliminary results of the ACSé phase II trial.J Clin Oncol. 2015;33:8065. [DOI]
Wu YL, Yang JCH, Kim DW, Lu S, Zhou J, Seto T, et al. Phase II study of crizotinib in East Asian patients with ROS1-positive advanced non–small-cell lung cancer.J Clin Oncol. 2018;36:1405–11. [DOI] [PubMed]
Raedler LA. Zykadia (ceritinib) approved for patients with crizotinib-resistant ALK -positive non-small-cell lung cancer.Am Health Drug Benefits. 2015;8:163–6. [PubMed] [PMC]
Morris TA, Khoo C, Solomon BJ. Targeting ROS1 rearrangements in non-small cell lung cancer: crizotinib and newer generation tyrosine kinase inhibitors.Drugs. 2019;79:1277–86. [DOI] [PubMed]
Roskoski R Jr. ROS1 protein-tyrosine kinase inhibitors in the treatment of ROS1 fusion protein-driven non-small cell lung cancers.Pharmacol Res. 2017;121:202–12. [DOI] [PubMed]
Lim SM, Kim HR, Lee JS, Lee KH, Lee YG, Min YJ, et al. Open-label, multicenter, phase II study of ceritinib in patients with non–small-cell lung cancer harboring ROS1 rearrangement.J Clin Oncol. 2017;35:2613–8. [DOI] [PubMed]
Awad MM, Katayama R, McTigue M, Liu W, Deng YL, Brooun A, et al. Acquired resistance to crizotinib from a mutation in CD74-ROS1.N Engl J Med. 2013;368:2395–401. [DOI] [PubMed] [PMC]
Katayama R, Kobayashi Y, Friboulet L, Lockerman EL, Koike S, Shaw AT, et al. Cabozantinib overcomes crizotinib resistance in ROS1 fusion–positive cancer.Clin Cancer Res. 2015;21:166–74. [DOI] [PubMed] [PMC]
Facchinetti F, Loriot Y, Kuo MS, Mahjoubi L, Lacroix L, Planchard D, et al. Crizotinib-resistant ROS1 mutations reveal a predictive kinase inhibitor sensitivity model for ROS1- and ALK-rearranged lung cancers.Clin Cancer Res. 2016;22:5983–91. [DOI] [PubMed]
Shaw AT, Ou SH, Bang YJ, Camidge DR, Solomon BJ, Salgia R, et al. Crizotinib in ROS1-rearranged non–small-cell lung cancer.N Engl J Med. 2014;371:1963–71. [DOI] [PubMed] [PMC]
Cho BC, Kim DW, Bearz A, Laurie SA, McKeage M, Borra G, et al. ASCEND-8: A randomized phase 1 study of ceritinib, 450 mg or 600 mg, taken with a low-fat meal versus 750 mg in fasted state in patients with anaplastic lymphoma kinase (ALK)-rearranged metastatic non–small cell lung cancer (NSCLC).J Thorac Oncol. 2017;12:1357–67. [DOI] [PubMed]
Mazières J, Zalcman G, Crinò L, Biondani P, Barlesi F, Filleron T, et al. Crizotinib therapy for advanced lung adenocarcinoma and a ROS1 rearrangement: results from the EUROS1 cohort.J Clin Oncol. 2015;33:992–9. [DOI] [PubMed]
Tappenden P, Carroll C, Hamilton J, Kaltenthaler E, Wong R, Wadsley J, et al. Cabozantinib and vandetanib for unresectable locally advanced or metastatic medullary thyroid cancer: a systematic review and economic model.Health Technol Assess. 2019;23:1–144. [DOI] [PubMed] [PMC]
Rolfo C, Ruiz R, Giovannetti E, Gil-Bazo I, Russo A, Passiglia F, et al. Entrectinib: a potent new TRK, ROS1, and ALK inhibitor.Expert Opin Investig Drugs. 2015;24:1493–500. [DOI] [PubMed]
Doebele R, Ahn M, Siena S, Drilon A, Krebs M, Lin C, et al. OA02.01 Efficacy and safety of entrectinib in locally advanced or metastatic ROS1 fusion-positive non-small cell lung cancer (NSCLC).J Thorac Oncol. 2018;13:S321–2. [DOI]
Demetri GD, Paz-Ares L, Farago AF, Liu SV, Chawla SP, Tosi D, et al. LBA17 Efficacy and safety of entrectinib in patients with NTRK fusion-positive (NTRK-fp) tumors: pooled analysis of STARTRK-2, STARTRK-1 and ALKA-372-001.Ann Oncol. 2018;29:VIII713. [DOI]
Drilon A, Siena S, Dziadziuszko R, Barlesi F, Krebs MG, Shaw AT, et al.; trial investigators. Entrectinib in ROS1 fusion-positive non-small-cell lung cancer: integrated analysis of three phase 1–2 trials.Lancet Oncol. 2020;21:261–70.Erratum in: Lancet Oncol. 2020;21:e70. Erratum in: Lancet Oncol. 2020;21:e341. [DOI] [PubMed] [PMC]
Azelby CM, Sakamoto MR, Bowles DW. ROS1 targeted therapies: current status.Curr Oncol Rep. 2021;23:94. [DOI] [PubMed]
Keddy C, Shinde P, Jones K, Kaech S, Somwar R, Shinde U, et al. Resistance profile and structural modeling of next-generation ROS1 tyrosine kinase inhibitors.Mol Cancer Ther. 2022;21:336–46. [DOI] [PubMed] [PMC]
Watanabe J, Furuya N, Fujiwara Y. Appearance of a BRAF mutation conferring resistance to crizotinib in non–small cell lung cancer harboring oncogenic ROS1 fusion.J Thorac Oncol. 2018;13:e66–9. [DOI] [PubMed]
Lin JJ, Johnson T, Lennerz JK, Lee C, Hubbeling HG, Yeap BY, et al. Resistance to lorlatinib in ROS1 fusion-positive non-small cell lung cancer.J Clin Oncol. 2020;38:9611. [DOI]
Otsu Y, Kata Y, Takayasu H, Inoue S, Kaneko T. Entrectinib-induced heart failure in a patient with metastatic lung adenocarcinoma: a case report.Cureus. 2022;14:e32174. [DOI] [PubMed] [PMC]
Pulciani S, Santos E, Lauver AV, Long LK, Aaronson SA, Barbacid M. Oncogenes in solid human tumours.Nature. 1982;300:539–42. [DOI] [PubMed]
Martin-Zanca D, Oskam R, Mitra G, Copeland T, Barbacid M. Molecular and biochemical characterization of the human trk proto-oncogene.Mol Cell Biol. 1989;9:24–33. [DOI] [PubMed] [PMC]
Klein R, Jing SQ, Nanduri V, O’Rourke E, Barbacid M. The trk proto-oncogene encodes a receptor for nerve growth factor.Cell. 1991;65:189–97. [DOI] [PubMed]
Kaplan DR, Hempstead BL, Martin-Zanca D, Chao MV, Parada LF. The trk proto-oncogene product: a signal transducing receptor for nerve growth factor.Science. 1991;252:554–8. [DOI] [PubMed]
Soppet D, Escandon E, Maragos J, Middlemas DS, Reid SW, Blair J, et al. The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor.Cell. 1991;65:895–903. [DOI] [PubMed]
Drilon A, Laetsch TW, Kummar S, DuBois SG, Lassen UN, Demetri GD, et al. Efficacy of larotrectinib in TRK fusion–positive cancers in adults and children.N Engl J Med. 2018;378:731–9. [DOI] [PubMed] [PMC]
Doebele RC, Drilon A, Paz-Ares L, Siena S, Shaw AT, Farago AF, et al.; trial investigators. Entrectinib in patients with advanced or metastatic NTRK fusion-positive solid tumours: integrated analysis of three phase 1–2 trials.Lancet Oncol. 2020;21:271–82.Erratum in: Lancet Oncol. 2020;21:e70. Erratum in: Lancet Oncol. 2020;21:e341. Erratum in: Lancet Oncol. 2020;21:e372. Erratum in: Lancet Oncol. 2021;22:e428. [DOI] [PubMed] [PMC]
Hong DS, Shen L, van Tilburg CM, Tan DSW, Kummar S, Lin JJ, et al. Long-term efficacy and safety of larotrectinib in an integrated dataset of patients with TRK fusion cancer.J Clin Oncol. 2021;39:3108. [DOI]
Lin JJ, Kummar S, Tan DSW, Lassen UN, Leyvraz S, Liu Y, et al. Long-term efficacy and safety of larotrectinib in patients with TRK fusion-positive lung cancer.J Clin Oncol. 2021;39:9109. [DOI]
Marinelli D, Siringo M, Metro G, Ricciuti B, Gelibter AJ. Non-small-cell lung cancer: how to manage ALK-, ROS1- and NTRK-rearranged disease.Drugs Context. 2022;11:2022-3-1. [DOI] [PubMed] [PMC]
Siena S, Doebele RC, Shaw AT, Karapetis CS, Tan DSW, Cho BC, et al. Efficacy of entrectinib in patients (pts) with solid tumors and central nervous system (CNS) metastases: integrated analysis from three clinical trials.J Clin Oncol. 2019;37:3017. [DOI]
Paz-Ares L, Barlesi F, Siena S, Ahn MJ, Drilon A, Conley A, et al. Patient-reported outcomes from STARTRK-2: a global phase II basket study of entrectinib for ROS1 fusion-positive non-small-cell lung cancer and NTRK fusion-positive solid tumours.ESMO Open. 2021;6:100113. [DOI] [PubMed] [PMC]
Doz F, van Tilburg CM, Geoerger B, Højgaard M, Øra I, Boni V, et al. Efficacy and safety of larotrectinib in TRK fusion-positive primary central nervous system tumors.Neuro Oncol. 2022;24:997–1007. [DOI] [PubMed] [PMC]
Murray BW, Rogers E, Zhai D, Deng W, Chen X, Sprengeler PA, et al. Molecular characteristics of repotrectinib that enable potent inhibition of TRK fusion proteins and resistant mutations.Mol Cancer Ther. 2021;20:2446–56. [DOI] [PubMed] [PMC]
Papadopoulos KP, Gandhi L, Janne PA, Ou SHI, Shaw A, Goldberg TR, et al. First-in-human study of DS-6051b in patients (pts) with advanced solid tumors (AST) conducted in the US.J Clin Oncol. 2018;36:2514. [DOI]
Ou Ignatius SH, Fujiwara Y, Shaw AT, Yamamoto N, Nakagawa K, Fan F, et al. Efficacy of taletrectinib (AB-106/DS-6051b) in ROS1+ NSCLC: an updated pooled analysis of U.S. and Japan phase 1 studies.JTO Clin Res Rep. 2020;2:100108. [DOI] [PubMed] [PMC]
Florou V, Nevala-Plagemann C, Whisenant J, Maeda P, Gilcrease GW, Garrido-Laguna I. Clinical activity of selitrectinib in a patient with mammary analogue secretory carcinoma of the parotid gland with secondary resistance to entrectinib.J Natl Compr Canc Netw. 2021;19:478–82. [DOI] [PubMed]
Hemming ML, Nathenson MJ, Lin JR, Mei S, Du Z, Malik K, et al. Response and mechanisms of resistance to larotrectinib and selitrectinib in metastatic undifferentiated sarcoma harboring oncogenic fusion of NTRK1.JCO Precis Oncol. 2020;4:79–90. [DOI] [PubMed] [PMC]
Russo M, Misale S, Wei G, Siravegna G, Crisafulli G, Lazzari L, et al. Acquired resistance to the TRK inhibitor entrectinib in colorectal cancer.Cancer Discov. 2016;6:36–44. [DOI] [PubMed]
Vaishnavi A, Scherzer MT, Kinsey CG, Parkman GL, Truong A, Ghazi P, et al. Inhibition of MEK1/2 forestalls the onset of acquired resistance to entrectinib in multiple models of NTRK1-driven cancer.Cell Rep. 2020;32:107994. [DOI] [PubMed] [PMC]
Hyman DM, Piha-Paul SA, Won H, Rodon J, Saura C, Shapiro GI, et al. HER kinase inhibition in patients with HER2- and HER3-mutant cancers.Nature. 2018;554:189–94.Erratum in: Nature. 2019;566:E11–2. [DOI] [PubMed] [PMC]
Drilon A, Cappuzzo F, Ou SHI, Camidge DR. Targeting MET in lung cancer: will expectations finally be MET?J Thorac Oncol. 2017;12:15–26. [DOI] [PubMed] [PMC]
Awad MM, Oxnard GR, Jackman DM, Savukoski DO, Hall D, Shivdasani P, et al. MET exon 14 mutations in non–small-cell lung cancer are associated with advanced age and stage-dependent MET genomic amplification and c-Met overexpression.J Clin Oncol. 2016;34:721–30. [DOI] [PubMed]
Tong JH, Yeung SF, Chan AWH, Chung LY, Chau SL, Lung RWM, et al. MET amplification and exon 14 splice site mutation define unique molecular subgroups of non–small cell lung carcinoma with poor prognosis.Clin Cancer Res. 2016;22:3048–56. [DOI] [PubMed]
Zhu YC, Wang WX, Xu CW, Zhang QX, Du KQ, Chen G, et al. Identification of a novel crizotinib-sensitive MET–ATXN7L1 gene fusion variant in lung adenocarcinoma by next generation sequencing.Ann Oncol. 2018;29:2392–3. [DOI] [PubMed]
Paik PK, Drilon A, Fan PD, Yu H, Rekhtman N, Ginsberg MS, et al. Response to MET inhibitors in patients with stage IV lung adenocarcinomas harboring MET mutations causing exon 14 skipping.Cancer Discov. 2015;5:842–9. [DOI] [PubMed] [PMC]
Paik PK, Felip E, Veillon R, Sakai H, Cortot AB, Garassino MC, et al. Tepotinib in non-small-cell lung cancer with MET exon 14 skipping mutations.N Engl J Med. 2020;383:931–43. [DOI] [PubMed] [PMC]
Wolf J, Seto T, Han JY, Reguart N, Garon EB, Groen HJM, et al.; GEOMETRY mono-1 Investigators. Capmatinib in MET exon 14–mutated or MET-amplified non–small-cell lung cancer.N Engl J Med. 2020;383:944–57. [DOI] [PubMed]
Wolf J, Seto T, Han JY, Reguart N, Garon EB, Groen HJM, et al. Capmatinib (INC280) in METΔex14-mutated advanced non-small cell lung cancer (NSCLC): efficacy data from the phase II GEOMETRY mono-1 study.J Clin Oncol. 2019;37:9004. [DOI]
Lu S, Fang J, Li X, Cao L, Zhou J, Guo Q, et al. Once-daily savolitinib in Chinese patients with pulmonary sarcomatoid carcinomas and other non-small-cell lung cancers harbouring MET exon 14 skipping alterations: a multicentre, single-arm, open-label, phase 2 study.Lancet Respir Med. 2021;9:1154–64. [DOI] [PubMed]
Drilon A, Clark JW, Weiss J, Ou SI, Camidge DR, Solomon BJ, et al. Antitumor activity of crizotinib in lung cancers harboring a MET exon 14 alteration.Nat Med. 2020;26:47–51. [DOI] [PubMed] [PMC]
Brazel D, Nagasaka M. Spotlight on amivantamab (JNJ-61186372) for EGFR exon 20 insertions positive non-small cell lung cancer.Lung Cancer (Auckl). 2021;12:133–8. [DOI] [PubMed] [PMC]
Guo A, Villén J, Kornhauser J, Lee KA, Stokes MP, Rikova K, et al. Signaling networks assembled by oncogenic EGFR and c-Met.Proc Natl Acad Sci U S A. 2008;105:692–7. [DOI] [PubMed] [PMC]
Dulak AM, Gubish CT, Stabile LP, Henry C, Siegfried JM. HGF-independent potentiation of EGFR action by c-Met.Oncogene. 2011;30:3625–35. [DOI] [PubMed] [PMC]
Bean J, Brennan C, Shih JY, Riely G, Viale A, Wang L, et al. MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib.Proc Natl Acad Sci U S A. 2007;104:20932–7. [DOI] [PubMed] [PMC]
Papadimitrakopoulou VA, Wu YL, Han JY, Ahn MJ, Ramalingam SS, John T, et al. LBA 51 Analysis of resistance mechanisms to osimertinib in patients with EGFR T790M advanced NSCLC from the AURA3 study.Ann Oncol. 2018;29:VIII741. [DOI]
Pasquini G, Giaccone G. C-MET inhibitors for advanced non-small cell lung cancer.Expert Opin Investig Drugs. 2018;27:363–75. [DOI] [PubMed]
Wu YL, Cheng Y, Zhou J, Lu S, Zhang Y, Zhao J, et al.; INSIGHT Investigators. Tepotinib plus gefitinib in patients with EGFR-mutant non-small-cell lung cancer with MET overexpression or MET amplification and acquired resistance to previous EGFR inhibitor (INSIGHT study): an open-label, phase 1b/2, multicentre, randomised trial.Lancet Respir Med. 2020;8:1132–43. [DOI] [PubMed]
Sequist LV, Han JY, Ahn MJ, Cho BC, Yu H, Kim SW, et al. Osimertinib plus savolitinib in patients with EGFR mutation-positive, MET-amplified, non-small-cell lung cancer after progression on EGFR tyrosine kinase inhibitors: interim results from a multicentre, open-label, phase 1b study.Lancet Oncol. 2020;21:373–86. [DOI] [PubMed]
Wu YL, Zhang L, Kim DW, Liu X, Lee DH, Yang JC, et al. Phase Ib/II study of capmatinib (INC280) plus gefitinib after failure of epidermal growth factor receptor (EGFR) inhibitor therapy in patients with EGFR-mutated, MET factor–dysregulated non–small-cell lung cancer.J Clin Oncol. 2018;36:3101–9.Erratum in: J Clin Oncol. 2019;37:261. [DOI] [PubMed]
Nishio M, Horiike A, Nokihara H, Horinouchi H, Nakamichi S, Wakui H, et al. Phase I study of the anti-MET antibody onartuzumab in patients with solid tumors and MET-positive lung cancer.Invest New Drugs. 2015;33:632–40. [DOI] [PubMed]
McCoach CE, Yu A, Gandara DR, Riess J, Li T, Mack PLC, et al. Phase I study of INC280 plus erlotinib in patients with MET expressing adenocarcinoma of the lung.J Clin Oncol. 2015;33:2587. [DOI]
Camidge DR, Moran T, Demedts I, Grosch H, Di Mercurio JP, Mileham KF, et al. A randomized, open-label, phase 2 study of emibetuzumab plus erlotinib (LY+E) and emibetuzumab monotherapy (LY) in patients with acquired resistance to erlotinib and MET diagnostic positive (MET Dx+) metastatic NSCLC.J Clin Oncol. 2016;34:9070. [DOI]
Guo R, Luo J, Chang J, Rekhtman N, Arcila M, Drilon A. MET-dependent solid tumours — molecular diagnosis and targeted therapy.Nat Rev Clin Oncol. 2020;17:569–87. [DOI] [PubMed] [PMC]
Camidge DR, Otterson GA, Clark JW, Ou SHI, Weiss J, Ades S, et al. Crizotinib in patients (pts) with MET-amplified non-small cell lung cancer (NSCLC): updated safety and efficacy findings from a phase 1 trial.J Clin Oncol. 2018;36:9062. [DOI]
Chen R, Manochakian R, James L, Azzouqa AG, Shi H, Zhang Y, et al. Emerging therapeutic agents for advanced non-small cell lung cancer.J Hematol Oncol. 2020;13:58. [DOI] [PubMed] [PMC]
Kohno T, Ichikawa H, Totoki Y, Yasuda K, Hiramoto M, Nammo T, et al. KIF5B-RET fusions in lung adenocarcinoma.Nat Med. 2012;18:375–7. [DOI] [PubMed] [PMC]
Takeuchi K, Soda M, Togashi Y, Suzuki R, Sakata S, Hatano S, et al. RET, ROS1 and ALK fusions in lung cancer.Nat Med. 2012;18:378–81. [DOI] [PubMed]
Sabari JK, Siau ED, Drilon A. Targeting RET-rearranged lung cancers with multikinase inhibitors.Oncoscience. 2017;4:23–4. [DOI] [PubMed] [PMC]
Drilon A, Rekhtman N, Arcila M, Wang L, Ni A, Albano M, et al. Cabozantinib in patients with advanced RET-rearranged non-small-cell lung cancer: an open-label, single-centre, phase 2, single-arm trial.Lancet Oncol. 2016;17:1653–60. [DOI] [PubMed] [PMC]
Yoh K, Seto T, Satouchi M, Nishio M, Yamamoto N, Murakami H, et al. Vandetanib in patients with previously treated RET-rearranged advanced non-small-cell lung cancer (LURET): an open-label, multicentre phase 2 trial.Lancet Respir Med. 2017;5:42–50. [DOI] [PubMed]
Hida T, Velcheti V, Reckamp KL, Nokihara H, Sachdev P, Kubota T, et al. A phase 2 study of lenvatinib in patients with RET fusion-positive lung adenocarcinoma.Lung Cancer. 2019;138:124–30. [DOI] [PubMed]
Gautschi O, Milia J, Filleron T, Wolf J, Carbone DP, Owen D, et al. Targeting RET in patients with RET-rearranged lung cancers: results from the global, multicenter RET registry.J Clin Oncol. 2017;35:1403–10. [DOI] [PubMed] [PMC]
Drilon A, Fu S, Patel MR, Fakih M, Wang D, Olszanski AJ, et al. A phase I/Ib trial of the VEGFR-sparing multikinase RET inhibitor RXDX-105.Cancer Discov. 2019;9:384–95. [DOI] [PubMed] [PMC]
Subbiah V, Gainor JF, Rahal R, Brubaker JD, Kim JL, Maynard M, et al. Precision targeted therapy with BLU-667 for RET-driven cancers.Cancer Discov. 2018;8:836–49. [DOI] [PubMed]
Gainor JF, Lee DH, Curigliano G, Doebele RC, Kim DW, Baik CS, et al. Clinical activity and tolerability of BLU-667, a highly potent and selective RET inhibitor, in patients (pts) with advanced RET-fusion+ non-small cell lung cancer (NSCLC).J Clin Oncol. 2019;37:9008. [DOI]
Drilon AE, Subbiah V, Oxnard GR, Bauer TM, Velcheti V, Lakhani NJ, et al. A phase 1 study of LOXO-292, a potent and highly selective RET inhibitor, in patients with RET-altered cancers.J Clin Oncol. 2018;36:102. [DOI]
Griesinger F, Curigliano G, Thomas M, Subbiah V, Baik CS, Tan DSW, et al. Safety and efficacy of pralsetinib in RET fusion-positive non-small-cell lung cancer including as first-line therapy: update from the ARROW trial☆.Ann Oncol. 2022;33:1168–78. [DOI] [PubMed]
Planchard D, Smit EF, Groen HJM, Mazieres J, Besse B, Helland Å, et al. Dabrafenib plus trametinib in patients with previously untreated BRAFV600E-mutant metastatic non-small-cell lung cancer: an open-label, phase 2 trial.Lancet Oncol. 2017;18:1307–16. [DOI] [PubMed]
Odogwu L, Mathieu L, Blumenthal G, Larkins E, Goldberg KB, Griffin N, et al. FDA approval summary: dabrafenib and trametinib for the treatment of metastatic non-small cell lung cancers harboring BRAF V600E mutations.Oncologist. 2018;23:740–5. [DOI] [PubMed] [PMC]
Bandola-Simon J, Roche PA. Dysfunction of antigen processing and presentation by dendritic cells in cancer.Mol Immunol. 2019;113:31–7. [DOI] [PubMed] [PMC]
He X, Xu C. Immune checkpoint signaling and cancer immunotherapy.Cell Res. 2020;30:660–9. [DOI] [PubMed] [PMC]
Okazaki T, Honjo T. PD-1 and PD-1 ligands: from discovery to clinical application.Int Immunol. 2007;19:813–24. [DOI] [PubMed]
Ishida Y. PD-1: its discovery, involvement in cancer immunotherapy, and beyond.Cells. 2020;9:1376. [DOI] [PubMed] [PMC]
Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy.Nat Rev Cancer. 2012;12:252–64. [DOI] [PubMed] [PMC]
La-Beck NM, Jean GW, Huynh C, Alzghari SK, Lowe DB. Immune checkpoint inhibitors: new insights and current place in cancer therapy.Pharmacotherapy. 2015;35:963–76.Erratum in: Pharmacotherapy. 2015;35:1205. [DOI] [PubMed]
Walker LS, Sansom DM. The emerging role of CTLA4 as a cell-extrinsic regulator of T cell responses.Nat Rev Immunol. 2011;11:852–63. [DOI] [PubMed]
Schadendorf D, Hodi FS, Robert C, Weber JS, Margolin K, Hamid O, et al. Pooled analysis of long-term survival data from phase II and phase III trials of ipilimumab in unresectable or metastatic melanoma.J Clin Oncol. 2015;33:1889–94. [DOI] [PubMed] [PMC]
Cascone T, William WN Jr, Weissferdt A, Leung CH, Lin HY, Pataer A, et al. Neoadjuvant nivolumab or nivolumab plus ipilimumab in operable non-small cell lung cancer: the phase 2 randomized NEOSTAR trial.Nat Med. 2021;27:504–14. [DOI] [PubMed] [PMC]
Brahmer J, Reckamp KL, Baas P, Crinò L, Eberhardt WE, Poddubskaya E, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer.N Engl J Med. 2015;373:123–35. [DOI] [PubMed] [PMC]
Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer.N Engl J Med. 2015;373:1627–39. [DOI] [PubMed] [PMC]
Vokes EE, Ready N, Felip E, Horn L, Burgio MA, Antonia SJ, et al. Nivolumab versus docetaxel in previously treated advanced non-small-cell lung cancer (CheckMate 017 and CheckMate 057): 3-year update and outcomes in patients with liver metastases.Ann Oncol. 2018;29:959–65. [DOI] [PubMed]
Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, et al.; KEYNOTE-001 Investigators. Pembrolizumab for the treatment of non-small-cell lung cancer.N Engl J Med. 2015;372:2018–28. [DOI] [PubMed]
Herbst RS, Baas P, Kim DW, Felip E, Pérez-Gracia JL, Han JY, et al. Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial.Lancet. 2016;387:1540–50. [DOI] [PubMed]
Reck M, Rodríguez-Abreu D, Robinson AG, Hui R, Csőszi T, Fülöp A, et al.; KEYNOTE-024 Investigators. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer.N Engl J Med. 2016;375:1823–33. [DOI] [PubMed]
Pai-Scherf L, Blumenthal GM, Li H, Subramaniam S, Mishra-Kalyani PS, He K, et al. FDA approval summary: pembrolizumab for treatment of metastatic non-small cell lung cancer: first-line therapy and beyond.Oncologist. 2017;22:1392–9. [DOI] [PubMed] [PMC]
Fehrenbacher L, Spira A, Ballinger M, Kowanetz M, Vansteenkiste J, Mazieres J, et al.; POPLAR Study Group. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): a multicentre, open-label, phase 2 randomised controlled trial.Lancet. 2016;387:1837–46. [DOI] [PubMed]
Rittmeyer A, Barlesi F, Waterkamp D, Park K, Ciardiello F, von Pawel J, et al.; OAK Study Group. Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial.Lancet. 2017;389:255–65.Erratum in: Lancet. 2017;389:e5. [DOI] [PubMed] [PMC]
Bordoni R, Ciardiello F, von Pawel J, Cortinovis D, Karagiannis T, Ballinger M, et al. Patient-reported outcomes in OAK: a phase III study of atezolizumab versus docetaxel in advanced non–small-cell lung cancer.Clin Lung Cancer. 2018;19:441–9.E4. [DOI] [PubMed]
Weinstock C, Khozin S, Suzman D, Zhang L, Tang S, Wahby S, et al. U.S. Food and Drug Administration approval summary: atezolizumab for metastatic non–small cell lung cancer.Clin Cancer Res. 2017;23:4534–9. [DOI] [PubMed]
Peters S, Gettinger S, Johnson ML, Jänne PA, Garassino MC, Christoph D, et al. Phase II trial of atezolizumab as first-line or subsequent therapy for patients with programmed death-ligand 1–selected advanced non–small-cell lung cancer (BIRCH).J Clin Oncol. 2017;35:2781–9.Erratum in: J Clin Oncol. 2018;36:931. [DOI] [PubMed] [PMC]
Socinski MA, Jotte RM, Cappuzzo F, Orlandi F, Stroyakovskiy D, Nogami N, et al.; IMpower150 Study Group. Atezolizumab for first-line treatment of metastatic nonsquamous NSCLC.N Engl J Med. 2018;378:2288–301. [DOI] [PubMed]
Cho BC, Abreu DR, Hussein M, Cobo M, Patel AJ, Secen N, et al. Tiragolumab plus atezolizumab versus placebo plus atezolizumab as a first-line treatment for PD-L1-selected non-small-cell lung cancer (CITYSCAPE): primary and follow-up analyses of a randomised, double-blind, phase 2 study.Lancet Oncol. 2022;23:781–92. [DOI] [PubMed]
Garassino MC, Cho BC, Kim JH, Mazières J, Vansteenkiste J, Lena H, et al.; ATLANTIC Investigators. Durvalumab as third-line or later treatment for advanced non-small-cell lung cancer (ATLANTIC): an open-label, single-arm, phase 2 study.Lancet Oncol. 2018;19:521–36. [DOI] [PubMed] [PMC]
Socinski MA, Özgüroğlu M, Villegas A, Daniel D, Vicente D, Murakami S, et al. Durvalumab after concurrent chemoradiotherapy in elderly patients with unresectable stage III non–small–cell lung cancer (PACIFIC).Clin Lung Cancer. 2021;22:549–61. [DOI] [PubMed]
Kazandjian D, Suzman DL, Blumenthal G, Mushti S, He K, Libeg M, et al. FDA approval summary: nivolumab for the treatment of metastatic non-small cell lung cancer with progression on or after platinum-based chemotherapy.Oncologist. 2016;21:634–42. [DOI] [PubMed] [PMC]
Francisco LM, Salinas VH, Brown KE, Vanguri VK, Freeman GJ, Kuchroo VK, et al. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells.J Exp Med. 2009;206:3015–29. [DOI] [PubMed] [PMC]
Gettinger SN, Horn L, Gandhi L, Spigel DR, Antonia SJ, Rizvi NA, et al. Overall survival and long-term safety of nivolumab (anti–programmed death 1 antibody, BMS-936558, ONO-4538) in patients with previously treated advanced non–small-cell lung cancer.J Clin Oncol. 2015;33:2004–12. [DOI] [PubMed] [PMC]
Rizvi NA, Mazières J, Planchard D, Stinchcombe TE, Dy GK, Antonia SJ, et al. Activity and safety of nivolumab, an anti-PD-1 immune checkpoint inhibitor, for patients with advanced, refractory squamous non-small-cell lung cancer (CheckMate 063): a phase 2, single-arm trial.Lancet Oncol. 2015;16:257–65. [DOI] [PubMed] [PMC]
Malik A, Kanneganti TD. Function and regulation of IL-1α in inflammatory diseases and cancer.Immunol Rev. 2018;281:124–37. [DOI] [PubMed] [PMC]
Allavena P, Mantovani A. Immunology in the clinic review series; focus on cancer: tumour-associated macrophages: undisputed stars of the inflammatory tumour microenvironment.Clin Exp Immunol. 2012;167:195–205. [DOI] [PubMed] [PMC]
Hong DS, Janku F, Naing A, Falchook GS, Piha-Paul S, Wheler JJ, et al. Xilonix, a novel true human antibody targeting the inflammatory cytokine interleukin-1 alpha, in non-small cell lung cancer.Invest New Drugs. 2015;33:621–31. [DOI] [PubMed] [PMC]
Pol JG, Caudana P, Paillet J, Piaggio E, Kroemer G. Effects of interleukin-2 in immunostimulation and immunosuppression.J Exp Med. 2020;217:e20191247. [DOI] [PubMed] [PMC]
Ridolfi L, Bertetto O, Santo A, Naglieri E, Lopez M, Recchia F, et al. Chemotherapy with or without low-dose interleukin-2 in advanced non-small cell lung cancer: results from a phase III randomized multicentric trial.Int J Oncol. 2011;39:1011–7. [DOI] [PubMed]
Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, Jung S, et al. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells.Cell. 2006;124:175–89.Erratum in: Cell. 2006;126:811. [DOI] [PubMed]
Li C, Fang R, Sun Y, Han X, Li F, Gao B, et al. Spectrum of oncogenic driver mutations in lung adenocarcinomas from East Asian never smokers.PLoS One. 2011;6:e28204. [DOI] [PubMed] [PMC]
Vicent S, Garayoa M, López-Picazo JM, Lozano MD, Toledo G, Thunnissen FB, et al. Mitogen-activated protein kinase phosphatase-1 is overexpressed in non-small cell lung cancer and is an independent predictor of outcome in patients.Clin Cancer Res. 2004;10:3639–49. [DOI] [PubMed]
Brognard J, Clark AS, Ni Y, Dennis PA. Akt/protein kinase B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to chemotherapy and radiation.Cancer Res. 2001;61:3986–97. [PubMed]
Jones DR, Broad RM, Madrid LV, Baldwin AS Jr, Mayo MW. Inhibition of NF-κB sensitizes non–small cell lung cancer cells to chemotherapy-induced apoptosis.Ann Thorac Surg. 2000;70:930–6. [DOI] [PubMed]
Karin M, Greten FR. NF-κB: linking inflammation and immunity to cancer development and progression.Nat Rev Immunol. 2005;5:749–59. [DOI] [PubMed]
Meylan E, Dooley AL, Feldser DM, Shen L, Turk E, Ouyang C, et al. Requirement for NF-κB signalling in a mouse model of lung adenocarcinoma.Nature. 2009;462:104–7. [DOI] [PubMed] [PMC]
Bassères DS, Ebbs A, Levantini E, Baldwin AS. Requirement of the NF-κB subunit p65/RelA for K-Ras–induced lung tumorigenesis.Cancer Res. 2010;70:3537–46. [DOI] [PubMed] [PMC]
Muthuswamy R, Berk E, Junecko BF, Zeh HJ, Zureikat AH, Normolle D, et al. NF-κB hyperactivation in tumor tissues allows tumor-selective reprogramming of the chemokine microenvironment to enhance the recruitment of cytolytic T effector cells.Cancer Res. 2012;72:3735–43. [DOI] [PubMed] [PMC]
Hopewell EL, Zhao W, Fulp WJ, Bronk CC, Lopez AS, Massengill M, et al. Lung tumor NF-κB signaling promotes T cell-mediated immune surveillance.J Clin Invest. 2013;123:2509–22. [DOI] [PubMed] [PMC]
Xia Y, Shen S, Verma IM. NF-κB, an active player in human cancers.Cancer Immunol Res. 2014;2:823–30. [DOI] [PubMed] [PMC]
Liu T, Zhang L, Joo D, Sun SC. NF-κB signaling in inflammation.Signal Transduct Target Ther. 2017;2:17023. [DOI]
Akca H, Demiray A, Tokgun O, Yokota J. Invasiveness and anchorage independent growth ability augmented by PTEN inactivation through the PI3K/AKT/NFkB pathway in lung cancer cells.Lung Cancer. 2011;73:302–9.Erratum in: Lung Cancer. 2016;101:147. [DOI] [PubMed]
Wu B, Chien EY, Mol CD, Fenalti G, Liu W, Katritch V, et al. Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists.Science. 2010;330:1066–71. [DOI] [PubMed] [PMC]
Chen ZJ. Ubiquitin signalling in the NF-κB pathway.Nat Cell Biol. 2005;7:758–65. [DOI] [PubMed] [PMC]
Zhu J, Luo J, Li Y, Jia M, Wang Y, Huang Y, et al. HMGB1 induces human non-small cell lung cancer cell motility by activating integrin αvβ3/FAK through TLR4/NF-κB signaling pathway.Biochem Biophys Res Commun. 2016;480:522–7. [DOI] [PubMed]
Zhang N, Shen J, Gou L, Cao M, Ding W, Luo P, et al. UBE3A deletion enhances the efficiency of immunotherapy in non-small-cell lung cancer.Bioengineered. 2022;13:11577–92. [DOI] [PubMed] [PMC]
Liu C, Zheng S, Wang Z, Wang S, Wang X, Yang L, et al. KRAS-G12D mutation drives immune suppression and the primary resistance of anti-PD-1/PD-L1 immunotherapy in non-small cell lung cancer.Cancer Commun (Lond). 2022;42:828–47. [DOI] [PubMed] [PMC]
Landre T, Justeau G, Assié JB, Chouahnia K, Davoine C, Taleb C, et al. Anti-PD-(L)1 for KRAS-mutant advanced non-small–cell lung cancers: a meta-analysis of randomized–controlled trials.Cancer Immunol Immunother. 2022;71:719–26. [DOI] [PubMed]
Ricciuti B, Wang X, Alessi JV, Rizvi H, Mahadevan NR, Li YY, et al. Association of high tumor mutation burden in non–small cell lung cancers with increased immune infiltration and improved clinical outcomes of PD-L1 blockade across PD-L1 expression levels.JAMA Oncol. 2022;8:1160–8.Erratum in: JAMA Oncol. 2022;8:1702. [DOI] [PubMed] [PMC]
Antonia S, Goldberg SB, Balmanoukian A, Chaft JE, Sanborn RE, Gupta A, et al. Safety and antitumour activity of durvalumab plus tremelimumab in non-small cell lung cancer: a multicentre, phase 1b study.Lancet Oncol. 2016;17:299–308. [DOI] [PubMed] [PMC]
Planchard D, Reinmuth N, Orlov S, Fischer JR, Sugawara S, Mandziuk S, et al. ARCTIC: durvalumab with or without tremelimumab as third-line or later treatment of metastatic non-small-cell lung cancer☆.Ann Oncol. 2020;31:609–18. [DOI] [PubMed]
Paz-Ares L, Ciuleanu TE, Cobo M, Schenker M, Zurawski B, Menezes J, et al. First-line nivolumab plus ipilimumab combined with two cycles of chemotherapy in patients with non-small-cell lung cancer (CheckMate 9LA): an international, randomised, open-label, phase 3 trial.Lancet Oncol. 2021;22:198–211.Erratum in: Lancet Oncol. 2021;22:e92. [DOI] [PubMed]
Shiraishi Y, Hakozaki T, Nomura S, Kataoka T, Tanaka K, Miura S, et al. A multicenter, randomized phase III study comparing platinum combination chemotherapy plus pembrolizumab with platinum combination chemotherapy plus nivolumab and ipilimumab for treatment-naive advanced non–small cell lung cancer without driver gene alterations: JCOG2007 (NIPPON Study).Clin Lung Cancer. 2022;23:E285–8. [DOI] [PubMed]
Zhou C, Wang Z, Sun Y, Cao L, Ma Z, Wu R, et al. Sugemalimab versus placebo, in combination with platinum-based chemotherapy, as first-line treatment of metastatic non-small-cell lung cancer (GEMSTONE-302): interim and final analyses of a double-blind, randomised, phase 3 clinical trial.Lancet Oncol. 2022;23:220–33. [DOI] [PubMed]
Malik P, Mukherjee TK. Recent advances in gold and silver nanoparticle based therapies for lung and breast cancers.Int J Pharm. 2018;553:483–509. [DOI] [PubMed]
Malik P, Ameta RK. Recent advances in Au NP strategies of lung cancers. In: Paul S, editor. Biomedical engineering and its applications in healthcare. Springer Nature Publications; 2019.
Malik P, Hoidal JR, Mukherjee TK. Recent advances in curcumin treated non-small cell lung cancers: an impetus of pleiotropic traits and nanocarrier aided delivery.Curr Med Chem. 2021;28:3061–106. [DOI] [PubMed]
Malik P, Gupta R, Malik V, Ameta RK. Emerging nanomaterials for improved biosensing.Meas Sensors. 2021;16:10050. [DOI]
