Genomic instability as a major mechanism for acquired resistance to EGFR tyrosine kinase inhibitors in cancer

References

[1] Aguilar-Serra J, Gimeno-Ballester V, Pastor-Clerigues A, Milara J, Marti-Bonmati E, Trigo-VicenteCAlós-Almiñana M, Cortijo J(2019) Osimertinib in first-line treatment of advanced EGFRmutated non-small-cell lung cancer: a cost-effectiveness analysis. J Comp Eff Res 8(11):853–863

[2] Awad MM, Leonardi GC, Kravets S, Dahlberg SE, Drilon A, Noonan SA, Camidge DR, Ou SI, Costa DB, Gadgeel SM (2019) Impact of MET inhibitors on survival among patients with nonsmall cell lung cancer harboring MET exon 14 mutations: a retrospective analysis. Lung Cancer 133:96–102

[3] Bandyopadhyay D, Mandal M, Adam L, Mendelsohn J, Kumar R(1998) Physical interaction between epidermal growth factor receptor and DNA-dependent protein kinase in mammalian cells. J Biol Chem 273(3):1568–1573

[4] Baraibar I, Mezquita L, Gil-Bazo I, Planchard D(2020) Novel drugs targeting EGFR and HER2 exon 20 mutations in metastatic NSCLC. Crit Rev Oncol Hematol 148:102906

[5] Bareschino MA, Schettino C, Troiani T, Martinelli E, Morgillo F, Ciardiello F(2007) Erlotinib in cancer treatment. Ann Oncol 18 (Suppl 6):vi35–vi41

[6] Bębenek A, Ziuzia-Graczyk I(2018) Fidelity of DNA replication-a matter of proofreading. Curr Genet 64(5):985–996

[7] Cao X, Zhou Y, Sun H, Xu M, Bi X, Zhao Z, Shen B, Wan F, Hong Z, Lan L(2018) EGFR-TKI-induced HSP70 degradation and BER suppression facilitate the occurrence of the EGFR T790 M resistant mutation in lung cancer cells. Cancer Lett 424:84–96

[8] Dittmann K, Mayer C, Fehrenbacher B, Schaller M, Raju U, Milas L, Chen DJ, Kehlbach R, Rodemann HP(2005a) Radiation-induced epidermal growth factor receptor nuclear import is linked to activation of DNA-dependent protein kinase. J Biol Chem 280 (35):31182–31189

[9] Dittmann K, Mayer C, Rodemann HP(2005b) Inhibition of radiationinduced EGFR nuclear import by C225 (Cetuximab) suppresses DNA-PK activity. Radiother Oncol 76(2):157–161

[10] Dittmann K, Mayer C, Kehlbach R, Rodemann HP(2008) Radiationinduced caveolin-1 associated EGFR internalization is linked with nuclear EGFR transport and activation of DNA-PK. Mol Cancer 7:69

[11] Dong RF, Zhu ML, Liu MM, Xu YT, Yuan LL, Bian J, Xia YZ, Kong LY(2021) EGFR mutation mediates resistance to EGFR tyrosine kinase inhibitors in NSCLC: from molecular mechanisms to clinical research. Pharmacol Res 167:105583

[12] Dungo RT, Keating GM(2013) Afatinib: first global approval. Drugs 73(13):1503–1515

[13] El Kadi N, Wang L, Davis A, Korkaya H, Cooke A, Vadnala V, Brown NA, Betz BL, Cascalho M, Kalemkerian GP(2018) The EGFR T790M mutation is acquired through AICDA-mediated deamination of 5-methylcytosine following TKI treatment in lung cancer. Cancer Res 78(24):6728–6735

[14] El-Hashim AZ, Khajah MA, Renno WM, Babyson RS, Uddin M, Benter IF, Ezeamuzie C, Akhtar S(2017) Src-dependent EGFR transactivation regulates lung inflammation via downstream signaling involving ERK1/2, PI3Kδ/Akt and NFκB induction in a murine asthma model. Sci Rep 7(1):9919

[15] Genova C, Rijavec E, Barletta G, Burrafato G, Biello F, Dal Bello MG, Coco S, Truini A, Alama A, Boccardo F(2014) Afatinib for the treatment of advanced non-small-cell lung cancer. Expert Opin Pharmacother 15(6):889–903

[16] Greig SL(2016) Osimertinib: first global approval. Drugs 76(2):263–273

[17] Haradhvala NJ, Kim J, Maruvka YE, Polak P, Rosebrock D, Livitz D, Hess JM, Leshchiner I, Kamburov A, Mouw KW(2018) Distinct mutational signatures characterize concurrent loss of polymerase proofreading and mismatch repair. Nat Commun 9 (1):1746

[18] Hata AN, Niederst MJ, Archibald HL, Gomez-Caraballo M, Siddiqui FM, Mulvey HE, Maruvka YE, Ji F, Bhang HE, Krishnamurthy Radhakrishna V(2016) Tumor cells can follow distinct evolutionary paths to become resistant to epidermal growth factor receptor inhibition. Nat Med 22(3):262–269

[19] Jin R, Zhao J, Xia L, Li Q, Li W, Peng L, Xia Y(2020) Application of immune checkpoint inhibitors in EGFR-mutant non-small-cell lung cancer: from bed to bench. Ther Adv Med Oncol 12:1758835920930333

[20] Johnson DB, Rioth MJ, Horn L(2014) Immune checkpoint inhibitors in NSCLC. Curr Treat Options Oncol 15(4):658–669

[21] Kim Y, Ko J, Cui Z, Abolhoda A, Ahn JS, Ou SH, Ahn MJ, Park K(2012) The EGFR T790M mutation in acquired resistance to an irreversible second-generation EGFR inhibitor. Mol Cancer Ther 11(3):784–791

[22] Lemmon MA, Schlessinger J, Ferguson KM(2014) The EGFR family: not so prototypical receptor tyrosine kinases. Cold Spring Harb Perspect Biol 6(4):a020768

[23] Li Z, Liu B, Jin W, Wu X, Zhou M, Liu VZ, Goel A, Shen Z, Zheng L, Shen B(2018) hDNA2 Nuclease/helicase promotes centromeric DNA replication and genome stability. EMBO J 37(14)

[24] Lo YH, Ho PC, Wang SC(2012) Epidermal growth factor receptor protects proliferating cell nuclear antigen from cullin 4A proteinmediated proteolysis. J Biol Chem 287(32):27148–27157

[25] Ludmann S, Marx A(2016) Getting it right: how DNA polymerases select the right nucleotide. Chimia (Aarau) 70(3):203–206

[26] Ma C, Wei S, Song Y(2011) T790M and acquired resistance of EGFR TKI: a literature review of clinical reports. J Thorac Dis 3 (1):10–18

[27] Majem M, Remon J(2013) Tumor heterogeneity: evolution through space and time in EGFR mutant non small cell lung cancer patients. Transl Lung Cancer Res 2(3):226–237

[28] Markham A(2020) Tepotinib: first approval. Drugs 80(8):829–833

[29] Mehlman C, Cadranel J, Rousseau-Bussac G, Lacave R, Pujals A, Girard N, Callens C, Gounant V, Théou-Anton N, Friard S(2019) Resistance mechanisms to osimertinib in EGFR-mutated advanced non-small-cell lung cancer: a multicentric retrospective French study. Lung Cancer 137:149–156

[30] Moldovan GL, Pfander B, Jentsch S(2007) PCNA, the maestro of the replication fork. Cell 129(4):665–679

[31] Molina-Vila MA, Bertran-Alamillo J, Mayo C, Rosell R(2009) Screening for EGFR mutations in lung cancer. Discov Med 8 (43):181–184

[32] Moy B, Kirkpatrick P, Kar S, Goss P(2007) Lapatinib. Nat Rev Drug Discov 6(6):431–432

[33] Muhsin M, Graham J, Kirkpatrick P(2003) Gefitinib. Nat Rev Drug Discov 2(7):515–516

[34] Nathanson DA, Gini B, Mottahedeh J, Visnyei K, Koga T, Gomez G, Eskin A, Hwang K, Wang J, Masui K(2014) Targeted therapy resistance mediated by dynamic regulation of extrachromosomal mutant EGFR DNA. Science 343(6166):72–76

[35] Ou SI, Agarwal N, Ali SM(2016) High MET amplification level as a resistance mechanism to osimertinib (AZD9291) in a patient that symptomatically responded to crizotinib treatment post-osimertinib progression. Lung Cancer 98:59–61

[36] Reckamp KL, Frankel PH, Ruel N, Mack PC, Gitlitz BJ, Li T, Koczywas M, Gadgeel SM, Cristea MC, Belani CP(2019) Phase II trial of cabozantinib plus erlotinib in patients with advanced epidermal growth factor receptor (EGFR)-mutant nonsmall cell lung cancer with progressive disease on epidermal growth factor receptor tyrosine kinase inhibitor therapy: a california cancer consortium phase II trial (NCI 9303). Front Oncol 9:132

[37] Rotow JK, Gui P, Wu W, Raymond VM, Lanman RB, Kaye FJ, Peled N, Fece de la Cruz F, Nadres B, Corcoran RB(2020) Cooccurring alterations in the RAS-MAPK pathway limit response to MET inhibitor treatment in MET Exon 14 skipping mutationpositive lung cancer. Clin Cancer Res 26(2):439–449

[38] Sequist LV, Besse B, Lynch TJ, Miller VA, Wong KK, Gitlitz B, Eaton K, Zacharchuk C, Freyman A, Powell C(2010) Neratinib, an irreversible pan-ErbB receptor tyrosine kinase inhibitor: results of a phase II trial in patients with advanced non-small-cell lung cancer. J Clin Oncol 28(18):3076–3083

[39] Shi Y, Zhang L, Liu X, Zhou C, Zhang S, Wang D, Li Q, Qin S, Hu C, Zhang Y(2013) Icotinib versus gefitinib in previously treated advanced non-small-cell lung cancer (ICOGEN): a randomised, double-blind phase 3 non-inferiority trial. Lancet Oncol 14 (10):953–961

[40] Taniguchi H, Yamada T, Wang R, Tanimura K, Adachi Y, Nishiyama A, Tanimoto A, Takeuchi S, Araujo LH, Boroni M(2019) AXL confers intrinsic resistance to osimertinib and advances the emergence of tolerant cells. Nat Commun 10(1):259

[41] Turner KM, Deshpande V, Beyter D, Koga T, Rusert J, Lee C, Li B, Arden K, Ren B, Nathanson DA (2017) Extrachromosomal oncogene amplification drives tumour evolution and genetic heterogeneity. Nature 543(7643):122–125

[42] Vendetti FP, Lau A, Schamus S, Conrads TP, O’Connor MJ, Bakkenist CJ(2015) The orally active and bioavailable ATR kinase inhibitor AZD6738 potentiates the anti-tumor effects of cisplatin to resolve ATM-deficient non-small cell lung cancer in vivo. Oncotarget 6(42):44289–44305

[43] Wang SC, Hung MC(2009) Nuclear translocation of the epidermal growth factor receptor family membrane tyrosine kinase receptors. Clin Cancer Res 15(21):6484–6489

[44] Wang SC, Nakajima Y, Yu YL, Xia W, Chen CT, Yang CC, McIntush EW, Li LY, Hawke DH, Kobayashi R(2006) Tyrosine phosphorylation controls PCNA function through protein stability. Nat Cell Biol 8(12):1359–1368

[45] Wang YN, Lee HH, Lee HJ, Du Y, Yamaguchi H, Hung MC(2012) Membrane-bound trafficking regulates nuclear transport of integral epidermal growth factor receptor (EGFR) and ErbB-2. J Biol Chem 287(20):16869–16879

[46] Wang YN, Wang H, Yamaguchi H, Lee HJ, Lee HH, Hung MC(2010) COPI-mediated retrograde trafficking from the Golgi to the ER regulates EGFR nuclear transport. Biochem Biophys Res Commun 399(4):498–504

[47] Watanabe M, Kawaguchi T, Isa S, Ando M, Tamiya A, Kubo A, Saka H, Takeo S, Adachi H, Tagawa T(2015) Ultra-sensitive detection of the pretreatment EGFR T790M mutation in non-small cell lung cancer patients with an EGFR-activating mutation using droplet digital PCR. Clin Cancer Res 21(15):3552–3560

[48] Waters KM, Liu T, Quesenberry RD, Willse AR, Bandyopadhyay S, Kathmann LE, Weber TJ, Smith RD, Wiley HS, Thrall BD (2012) Network analysis of epidermal growth factor signaling using integrated genomic, proteomic and phosphorylation data. PLoS ONE 7(3):e34515

[49] Wu YL, Cheng Y, Zhou X, Lee KH, Nakagawa K, Niho S, Tsuji F, Linke R, Rosell R, Corral J(2017) Dacomitinib versus gefitinib as first-line treatment for patients with EGFR-mutation-positive nonsmall-cell lung cancer (ARCHER 1050): a randomised, open-label, phase 3 trial. Lancet Oncol 18(11):1454–1466

[50] Xing X, Kane DP, Bulock CR, Moore EA, Sharma S, Chabes A, Shcherbakova PV (2019) A recurrent cancer-associated substitution in DNA polymerase ε produces a hyperactive enzyme. Nat Commun 10(1):374

[51] Yu D, Zhao W, Vallega KA, Sun SY(2021) Managing acquired resistance to third-generation EGFR tyrosine kinase inhibitors through co-targeting MEK/ERK signaling. Lung Cancer (Auckl) 12:1–10

[52] Zhang H(2016a) Osimertinib making a breakthrough in lung cancer targeted therapy. Onco Targets Ther 9:5489–5493

[53] Zhang H(2016b) Three generations of epidermal growth factor receptor tyrosine kinase inhibitors developed to revolutionize the therapy of lung cancer. Drug Des Devel Ther 10:3867–3872

[54] Zheng L, Shen B(2011) Okazaki fragment maturation: nucleases take centre stage. J Mol Cell Biol 3(1):23–30

[55] Zheng L, Meng Y, Campbell JL, Shen B (2020) Multiple roles of DNA2 nuclease/helicase in DNA metabolism, genome stability and human diseases. Nucleic Acids Res 48(1):16–35

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