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Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

CN 11-5983/R

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Front. Med.    2023, Vol. 17 Issue (1) : 18-42    https://doi.org/10.1007/s11684-022-0976-4
REVIEW
Treatment of advanced non-small cell lung cancer with driver mutations: current applications and future directions
Jia Zhong, Hua Bai, Zhijie Wang, Jianchun Duan, Wei Zhuang, Di Wang, Rui Wan, Jiachen Xu, Kailun Fei, Zixiao Ma, Xue Zhang, Jie Wang()
State Key Laboratory of Molecular Oncology, Department of Medical Oncology, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, China
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Abstract

With the improved understanding of driver mutations in non-small cell lung cancer (NSCLC), expanding the targeted therapeutic options improved the survival and safety. However, responses to these agents are commonly temporary and incomplete. Moreover, even patients with the same oncogenic driver gene can respond diversely to the same agent. Furthermore, the therapeutic role of immune-checkpoint inhibitors (ICIs) in oncogene-driven NSCLC remains unclear. Therefore, this review aimed to classify the management of NSCLC with driver mutations based on the gene subtype, concomitant mutation, and dynamic alternation. Then, we provide an overview of the resistant mechanism of target therapy occurring in targeted alternations (“target-dependent resistance”) and in the parallel and downstream pathways (“target-independent resistance”). Thirdly, we discuss the effectiveness of ICIs for NSCLC with driver mutations and the combined therapeutic approaches that might reverse the immunosuppressive tumor immune microenvironment. Finally, we listed the emerging treatment strategies for the new oncogenic alternations, and proposed the perspective of NSCLC with driver mutations. This review will guide clinicians to design tailored treatments for NSCLC with driver mutations.
Keywords non-small cell lung cancer      driver mutations      treatment strategy      resistant mechanism      immune-checkpoint inhibitors     
Corresponding Author(s): Jie Wang   
Just Accepted Date: 17 January 2023   Online First Date: 23 February 2023    Issue Date: 15 March 2023
 Cite this article:   
Jia Zhong,Hua Bai,Zhijie Wang, et al. Treatment of advanced non-small cell lung cancer with driver mutations: current applications and future directions[J]. Front. Med., 2023, 17(1): 18-42.
 URL:  
https://academic.hep.com.cn/fmd/EN/10.1007/s11684-022-0976-4
https://academic.hep.com.cn/fmd/EN/Y2023/V17/I1/18
Fig.1  Stratified management of NSCLC with driver mutations (take EGFR mutation as an example).
Drugs Resistant mechanism Possible solutions References
EGFR
First- or second-generation EGFR-TKIs Target-dependent resistance T790M Third generation EGFR-TKIs Cross et al. [121]
Target-independent resistance MET amplification/ skip mutation EGFR-TKIs + MET inhibitor Giroux-Leprieur et al. [122]
RET fusion EGFR-TKIs + RET inhibitor Piotrowska et al. [123]
BRAF mutation, HER-2 mutation and amplification EGFR-TKIs + BRAF/HER-2 inhibitor Wu et al. [124]
Other resistant mechanisms Histologic transformation Etopside + platinum Marcoux et al. [125]
Third-generation EGFR-TKIs Target-dependent resistance C797S in trans Osimertinib + first generation EGFR-TKIs Arulananda et al. [126]
C797S in cis Osimertinib + bevacizumab + brigatinib Zhao et al. [127]
EGFR amplifications and mutations EGFR/MET bispecific monoclonal antibody (amivantamab) Shah et al. [86],Scalvini et al. [128]
Target-independent resistance MET amplification Osimertinib + MET inhibitors, or amivantamab Giroux-Leprieur et al. [122],Neijssen et al. [129]
BRAF mutation or NF1 mutation that leads to activation of MAPK pathway Combined MEK and EGFR-TKIs Tricker et al. [98]
Loss of PTEN and PIK3CA mutation PI3K-AKT-mTOR pathway inhibitors Sato et.al. [130]
Her-2 mutation and amplification HER-2 inhibitors Zhou et.al. [131]
SRC activation SRC inhibitor dasatinib Watanabe et al. [132]
AXL overexpression AXL-TKIs Okura et al. [133]
Cell cycle alternations (CCND1 amplification, CCND2 amplification, CKD6 amplification, CCKE1 amplification) No evidence Cho et al. [134]
Other resistant mechanisms SCLC/SCC transformation Etopside + platinum/chemotherapy for SCC Yin et al. [135,136]
ALK
First generation ALK-TKIs Target-dependent resistance ALK copy number gain Second generation ALK-TKIs Russo et al. [137]
L1196M, C1156Y, 1151Tins, L1152R, G1202R, D1203N, S1206 Y, G1269A, G1128A, I1171T, E1210K, C1156S, F1245V Second generation ALK-TKIs (G1202R only sensitive to brigatinib and lorlatinib) Russo et al. [137]
Target-independent resistance KIT amplification, KRAS mutations, EGFR mutation and/or amplification, IGF-1R activation, RAS/MEK activation No evidence Russo et al. [137]
Other resistant mechanisms SCLC/EMT transformation Etopside + platinum Russo et al. [137]
Second generation ALK-TKIs Target-dependent resistance G1202R, I1171; F1174 (resistant to ceritinib but sensitive to alectinib) Lorlatinib Shaw et al. [138]
Target-independent resistance MET amplification, RAS/MEK activation, protein kinase C (PKC) activation, SRC activation, activation of EGFR and HER4 pathways, SHP2 activation, and NF2 loss No evidence Russo et al. [137]
Third generation ALK-TKIs Target-dependent resistance Compound mutations such as G1202R + L1196M, D1203N + F1174C, D1203N + E1210K Rechallenge with 1st/2nd generation ALK-TKIs 4th generation TKI: TPX0131 has potency against wild-type (WT) ALK and a spectrum of acquired resistance mutations Russo et al. [137],Yoda et al. [137],Takahashi et al. [137],Murray et al. [139]
Target-independent resistance MET amplification ALK-TKI + MEK inhibitors Dagogo-Jack et al. [140]
ROS-1
Crizotinib Target-dependent resistance L2026M No evidence Mccoach et al. [141]
ROS1-G2032R,D2033N, S1986F/Y G2032R mutation tumors was inhibited by repotrectinib, S1986F/Y mutation tumors was inhibited by lorlatinib [142] Katayama et al. [143],Drilon et al. [144],Gainor et al. [145]
Target-independent resistance KRAS G12C and NRAS Q61K No evidence Cui et al. [146]
Kit mutation (D816G) No evidence Cui et al. [146]
RET
Selpercatinib/pralsetinib Target-dependent resistance RET G810R/S/C/V No evidence Lin et al. [89]
Target-independent resistance MET amplification No evidence Subbiah et al. [147]
KRAS amplification/PIK3CA mutation No evidence Nelson-Taylor et al. [148]
Vandetanib/cabozantinib Target-dependent resistance RET V804M Selpercatinib Drusbosky et al. [149]
BRAF
Dabrafenib + trametinib Target-dependent resistance BRAF splice variants or BRAF amplification No evidence Shimizu et al. [150]
BRAF fusion genes No evidence Kulkarni et al. [151]
Target-independent resistance Reactivation of RAS-RAF-MEK-ERK pathway, such as NRAS/KRAS or MEK 1/2 mutations No evidence Johnson et al. [152]
Activation of PI3K-AKT pathway, such as AKT activating mutations and PTEN loss of function No evidence Proietti et al. [153]
TP53, CDKN2A, KRAS G12D No evidence Rudin et al. [154]
MET
Type Ia (crizotinib) Target-dependent resistance V1092I/L, G1163R, D1164G, L1195V, D1228X, Y1230X No evidence Fujino et al. [154],Ou et al. [154]
Target-independent resistance HER-2 amplification, KRAS amplification. EGFR amplification No evidence Ding et al. [155],Bahcall et al. [156],Dagogo-Jack et al. [157]
Type Ib (topotinib, savolitinib, capmatinib) Target-dependent resistance D1228H/N, Y1230C/H/S MET V1092L, D1228G or Y1230H can benefit from type II MET inhibitors Yu et al. [158],Shen et al. [159]
Target-independent resistance KRAS, NRAS, BRAF, PIK3CA, FGF19, TP53 No evidence Guo et al. [160]
Type II (cabozantinib) Target-dependent resistance D1133V, Y1159H, L1195F, F1200I/L No evidence Fujino et al. [106]
HER2 20 insertion
Poziotinib Target-dependent resistance C805S HSP90 inhibitors Koga et al. [161]
Target-dependent resistance HER2 copy number gain HER2 targeted therapy: trastuzumab, afatinib, ado-trastuzumab emtansine Chuang et al. [162]
EGFR-TKIs (elotinib, afatinib, osimertinib) Target-dependent resistance HER2 mutations A775_G776insYVMA (YVMA) Poziotinib Koga et al. [161]
Lapatinib Target-dependent resistance L755P/S, T798M mutation in HER2 No evidence Yu et al. [163]
KRAS G12C
Sotorasib Target-dependent resistance KRAS Y96C/D/S, R68S/M, G12D/R/V/W, G13D, A59S, A59T The G13D, R68M, A59S, and A59T mutation is sensitive to adagrasib. Combination of BI-3406 (SOS1 inhibitor) and trametinib had potent activity against Y96D/S mutation. Novel KRAS inhibitor RM-018 overcomes KRAS G12C/Y96D Tanaka et al. [90],Awad et al. [91],Koga et al. [92]
Target-independent resistance NRAS (Q61K or G13R), MRAS (Q71R), BRAF (G596R), EGFR (amplification, P1108L and S1046R), FGFR2 (amplification, A68T and D304N) No evidence Zhao et al. [103]
MET amplification A combination of sotorasib and MET inhibitors such as crizotinib and capmatinib Zhao et al. [103],Suzuki et al. [105]
HER2 amplification A combination of sotorasib and SHP2 inhibitors Ho et al. [104]
Adagrasib Target-dependent resistance KRAS Y96C/D/S/, R68S Combination of BI-3406 and trametinib had potent activity against Y96D/S. RM-018 overcomes KRAS G12C/Y96D Tanaka et al. [90],Awad et al. [91],Koga et al. [92]
KRAS G12C amplification No evidence Awad et al. [91]
Target-independent resistance NRAS Q61L/R/K, BRAF V600E, MAP2K1 Q56P, MAP2K1 E102_103/104del, PIK3CA H1047R, RET M918T, MET amplification, EML4-ALK and FGFR3- TACC3, etc. No evidence Awad et al. [91]
Other resistant mechanism Squamous cell transformation No evidence Awad et al. [91]
NTRK fusion
Larotrectinib or entrectinib Target-dependent resistance Solvent front, gatekeeper residue and xDFG motif No evidence Russo et al. [137],Cocco et al. [191]
Target-independent resistance KRAS mutation, MET amplification, BRAF mutation No evidence Cocco et al. [191]
Tab.1  Summary of resistant mechanisms for target therapy in lung cancer
Fig.2  Potential mechanisms of low ICI efficacy in EGFR mutant NSCLC. Abbreviations: CXCL10, CXC-chemokine ligand 10; PI3K, phosphatidylinositol-3 kinase; CCL22, CC-chemokine ligand 22; Treg, T-regulatory cell; NK cell, natural killer cell; M1, macrophages 2; M2, macrophages 2; ATP, adenosine triphosphate; ADO, adenosine.
Target Genomic alternation Treatment NCT number
EGFR Mutation Bispecific antibody targeting EGFR and MET (amivantamab, etc.) NCT02609776
Fourth generation EGFR-TKIs (BLU-945, etc.) NCT04862780
CD73-adenosine axis blocked + PD-(L)1 NCT05431270NCT03454451NCT05221840
CD73-adenosine axis blocked + EGFR-TKIs NCT03381274
EGFR CAR-T cells NCT03198052
ALK Fusion Double mutant active fourth generation ALK-TKIs (TPX-0131 and NVL-655) NCT04849273NCT05384626
KRAS Mutation KRAS inhibitor sotorasib or adagrasib combination therapy (PD-(L)1/EGFR antibody, etc.) NCT03785249NCT04185883
KRAS inhibitor + RAF/MEK inhibitor (VS-6766) NCT05375994
RET Fusion RET/SRC inhibitor (TPX-0046) NCT04161391
ROS-1, NTRK Fusion Target solvent-front mutations (repotrectinib) NCT04772235
MET Mutation and amplification MET ADC (ABBV-399) NCT03539536NCT02099058
Bispecific antibody targeting EGFR and MET (amivantamab, etc.) NCT02609776
HER2 Mutation and overexpression HER2 ADC (TDM1, DS-8201) + PD-(L)1 + chemotherapy NCT04686305NCT04042701
HER3 Overexpression HER3 ADC (patritumab deruxtecan) + EGFR-TKIs NCT04676477
SHP-2 Overexpression SHP-2 inhibitor + PD-(L)1/KRAS inhibitor NCT05375084NCT05480865
NRG1 Fusion HER2×HER3 bispecific antibody (zenocutuzumab) NCT02912949
Tab.2  Emerging treatment for NSCLC with driver mutations
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2 LV Sequist, JCH Yang, N Yamamoto, K O’Byrne, V Hirsh, T Mok, SL Geater, S Orlov, CM Tsai, M Boyer, WC Su, J Bennouna, T Kato, V Gorbunova, KH Lee, R Shah, D Massey, V Zazulina, M Shahidi, M Schuler. Phase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutations. J Clin Oncol 2013; 31(27): 3327–3334
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3 TS Mok, YL Wu, MJ Ahn, MC Garassino, HR Kim, SS Ramalingam, FA Shepherd, Y He, H Akamatsu, WS Theelen, CK Lee, M Sebastian, A Templeton, H Mann, M Marotti, S Ghiorghiu, VA; AURA3 Investigators Papadimitrakopoulou. Osimertinib or platinum-pemetrexed in EGFR T790M-positive lung cancer. N Engl J Med 2017; 376(7): 629–640
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4 L Friboulet, N Li, R Katayama, CC Lee, JF Gainor, AS Crystal, PY Michellys, MM Awad, N Yanagitani, S Kim, AC Pferdekamper, J Li, S Kasibhatla, F Sun, X Sun, S Hua, P McNamara, S Mahmood, EL Lockerman, N Fujita, M Nishio, JL Harris, AT Shaw, JA Engelman. The ALK inhibitor ceritinib overcomes crizotinib resistance in non-small cell lung cancer. Cancer Discov 2014; 4(6): 662–673
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5 JF Gainor, L Dardaei, S Yoda, L Friboulet, I Leshchiner, R Katayama, I Dagogo-Jack, S Gadgeel, K Schultz, M Singh, E Chin, M Parks, D Lee, RH DiCecca, E Lockerman, T Huynh, J Logan, LL Ritterhouse, LP Le, A Muniappan, S Digumarthy, C Channick, C Keyes, G Getz, D Dias-Santagata, RS Heist, J Lennerz, LV Sequist, CH Benes, AJ Iafrate, M Mino-Kenudson, JA Engelman, AT Shaw. Molecular mechanisms of resistance to first- and second-generation ALK inhibitors in ALK-rearranged lung cancer. Cancer Discov 2016; 6(10): 1118–1133
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6 S Zhang, R Anjum, R Squillace, S Nadworny, T Zhou, J Keats, Y Ning, SD Wardwell, D Miller, Y Song, L Eichinger, L Moran, WS Huang, S Liu, D Zou, Y Wang, Q Mohemmad, HG Jang, E Ye, N Narasimhan, F Wang, J Miret, X Zhu, T Clackson, D Dalgarno, WC Shakespeare, VM Rivera. The potent ALK inhibitor brigatinib (AP26113) overcomes mechanisms of resistance to first- and second-generation ALK inhibitors in preclinical models. Clin Cancer Res 2016; 22(22): 5527–5538
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7 S Peters, DR Camidge, AT Shaw, S Gadgeel, JS Ahn, DW Kim, SI Ou, M Pérol, R Dziadziuszko, R Rosell, A Zeaiter, E Mitry, S Golding, B Balas, J Noe, PN Morcos, T; ALEX Trial Investigators Mok. Alectinib versus crizotinib in untreated ALK-positive non-small-cell lung cancer. N Engl J Med 2017; 377(9): 829–838
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8 AT Shaw, TM Bauer, Marinis F de, E Felip, Y Goto, G Liu, J Mazieres, DW Kim, T Mok, A Polli, H Thurm, AM Calella, G Peltz, BJ; CROWN Trial Investigators Solomon. First-line lorlatinib or crizotinib in advanced ALK-positive lung cancer. N Engl J Med 2020; 383(21): 2018–2029
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9 DR Camidge, HR Kim, MJ Ahn, JCH Yang, JY Han, MJ Hochmair, KH Lee, A Delmonte, MR Garcia Campelo, DW Kim, F Griesinger, E Felip, R Califano, AI Spira, SN Gettinger, M Tiseo, HM Lin, Y Liu, F Vranceanu, H Niu, P Zhang, S Popat. Brigatinib versus crizotinib in ALK inhibitor-naive advanced ALK-positive NSCLC: final results of phase 3 ALTA-1L trial. J Thorac Oncol 2021; 16(12): 2091–2108
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10 BJ Solomon, T Mok, DW Kim, YL Wu, K Nakagawa, T Mekhail, E Felip, F Cappuzzo, J Paolini, T Usari, S Iyer, A Reisman, KD Wilner, J Tursi, F; PROFILE 1014 Investigators Blackhall. First-line crizotinib versus chemotherapy in ALK-positive lung cancer. N Engl J Med 2014; 371(23): 2167–2177
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