Heterogeneous mechanisms of primary and acquired resistance to third-generation EGFR inhibitors

Clinical Cancer Research

Volumn 22, Issue 19, 2016, Pages 4837-4847

  Ortiz Cuaran, Sandra ^a   Scheffler, Matthias ^b   Plenker, Dennis ^a,b   Dahmen, Llona ^a   Scheel, Andreas H ^b   Fernandez Cuesta, Lynnette ^a,c   Meder, Lydia ^b   Lovly, Christine M ^d   Persigehl, Thorsten ^b   Merkelbach Bruse, Sabine ^b   Bos, Marc ^a   Michels, Sebastian ^b   Fischer, Rieke ^b   Albus, Kerstin ^b   König, Katharina ^e   Schildhaus, Hans Ulrich ^f   Fassunke, Jana ^b   Ihle, Michaela A ^b   Pasternack, Helen ^b,g   Heydt, Carina ^b   Becker, Christian ^a   Altmüller, Janine ^a   Ji, Hongbin ^h,i   Müller, Christian ^a   Florin, Alexandra ^b   Heuckmann, Johannes M ^j   Nuernberg, Peter ^a   Ans, Sascha ^b   Heukamp, Lukas C ^b,j   Berg, Johannes ^k   Pao, William ^d   Peifer, Martin ^a,k   Buettner, Reinhard ^b   Wolf, Jürgen ^b   Thomas, Roman K ^a,b   Sos, Martin L ^b   more..

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^c INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^d VANDERBILT UNIVERSITY   (United States)

^e Labor Dr Quade und Kollegen GmbH   (Germany)

^f UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^g Leibniz Research Center Borstel   (Germany)

^h INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

ⁱ SHANGHAITECH UNIVERSITY   (China)

^j NEO New Oncology GmbH   (Germany)

^k UNIVERSITY OF COLOGNE   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CRIZOTINIB; OSIMERTINIB; ROCILETINIB; ACRYLAMIDE DERIVATIVE; ANILINE DERIVATIVE; ANTINEOPLASTIC AGENT; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; PYRIMIDINE DERIVATIVE;

ADULT; AGED; ARTICLE; CELL VIABILITY; CLINICAL ARTICLE; CYTOTOXICITY; DISEASE COURSE; DRUG MECHANISM; ENZYME INHIBITION; ERBB2 GENE; FEMALE; GENE ACTIVATION; GENE AMPLIFICATION; GENE MUTATION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LUNG ADENOCARCINOMA; MALE; MET GENE; ONCOGENE; ONCOGENE K RAS; PRIORITY JOURNAL; TUMOR BIOPSY; ADENOCARCINOMA; ANTAGONISTS AND INHIBITORS; DRUG RESISTANCE; GENETICS; LUNG TUMOR; MIDDLE AGED;

ACRYLAMIDES; ADENOCARCINOMA; AGED; ANILINE COMPOUNDS; ANTINEOPLASTIC AGENTS; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; LUNG NEOPLASMS; MALE; MIDDLE AGED; PYRIMIDINES; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 84991241383     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-1915     Document Type: Article

References (43)

1. Ohashi K, Maruvka YE, Michor F, Pao W. Epidermal growth factor receptor tyrosine kinase inhibitor-resistant disease. J Clin Oncol 2013; 31:1070-80.
2. Pao W, Miller VA, Politi KA, Riely GJ, Somwar R, Zakowski MF, et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2005;2:e73.
3. Kobayashi S, Boggon TJ, DayaramT, Jänne PA, KocherO,MeyersonM, et al. EGFR mutation and resistance of non-small cell lung cancer to gefitinib. N Engl J Med 2005;352:786-92.
4. Yun C-H, Mengwasser KE, Toms A V, WooMS, Greulich H, Wong K-K, et al. The T790M mutation in EGFR kinase causes drug resistance by increasingthe affinity for ATP. Proc Natl Acad Sci U S A 2008;105:2070-5.
5. Walter AO, Sjin RTT, Haringsma HJ, Ohashi K, Sun J, Lee K, et al. Discovery of a mutant-selective covalent inhibitor of EGFR that overcomes T790Mmediated resistance in NSCLC. Cancer Discov 2013;3:1404-15.
6. Cross DAE, Ashton SE, Ghiorghiu S, Eberlein C, Nathan CA, Spitzler PJ, et al. AZD9291, an irreversible EGFR TKI, overcomes T790M-mediated resistance to EGFR inhibitors in lung cancer. Cancer Discov 2014;4: 1046-61.
7. Jänne PA, Yang JC-H, Kim D-W, Planchard D, Ohe Y, Ramalingam SS, et al. AZD9291 in EGFR inhibitor-resistant non-small-cell lung cancer. N Engl J Med 2015;372:1689-99.
8. Sequist LV, Soria J-C, Goldman JW, Wakelee HA, Gadgeel SM, Varga A, et al. Rociletinib in EGFR-mutated non-small cell lung cancer. N Engl J Med 2015;372:1700-9.
9. Jänne PA, Ahn M, KimD, Kim S, Planchard D, Ramalingam S., et al. et al.A phase I study of AZD9291 in patients with EGFR-TKI-resistant advanced NSCLC-updated progression free survival and duration of response data. Geneva, Switzerland: European Lung Cancer Conference; 2015.
10. Thress KS, Paweletz CP, Felip E, Cho BC, Stetson D, Dougherty B, et al. Acquired EGFR C797S mutation mediates resistance to AZD9291 in non- small cell lung cancer harboring EGFR T790M. Nat Med 2015;21:560-2.
11. Yu HA, Tian SK, Drilon AE, Borsu L, Riely GJ, Arcila ME, et al. Acquired resistance of EGFR- mutant lung cancer to a T790M-specific EGFR inhibitor. JAMA Oncol 2015;1:982-4.
12. Eberlein CA, StetsonD,Markovets AA, Al-Kadhimi KJ, Lai Z, Fisher PR, et al. Acquired resistance to mutant-selective EGFR inhibitor AZD9291 is associated with increased dependence on RAS signaling in preclinical models. Cancer Res 2015;75:2489-500
13. Ercan D, Xu C, Yanagita M, Monast CS, Pratilas CA, Montero J, et al. Reactivation of ERK signaling causes resistance to EGFR kinase inhibitors. Cancer Discov 2012;2:934-47.
14. Hata AN, Niederst MJ, Archibald HL, Gomez-Caraballo M, Siddiqui FM, Mulvey HE, et al. Tumor cells can follow distinct evolutionary paths to become resistant to epidermal growth factor receptor inhibition. Nat Med 2016;22:262-9.
15. Tam IYS, Chung LP, Suen WS, Wang E, Wong MCM, Ho KK, et al. Distinct epidermal growth factor receptor and KRAS mutation patterns in non- small cell lung cancer patients with different tobacco exposure and clinicopathologic features. Clin Cancer Res 2006;12:1647-53.
16. Unni AM, Lockwood WW, Zejnullahu K, Lee-Lin S-Q, Varmus H. Evidence that synthetic lethality underlies the mutual exclusivity of oncogenic KRAS and EGFR mutations in lung adenocarcinoma. Elife 2015;4:e06907.
17. Schildhaus H-U, Schultheis AM, Rüschoff J, Binot E, Merkelbach-Bruse S, Fassunke J, et al. MET amplification status in therapy-nave adeno- and squamous cell carcinomas of the lung. Clin Cancer Res 2015;21:907-15.
18. Rüschoff J, Hanna W, Bilous M, Hofmann M, Osamura RY, Penault-Llorca F, et al. HER2 testing in gastric cancer: a practical approach. Mod Pathol 2012;25:637-50.
19. König K, Peifer M, Fassunke J, Ihle MA, Künstlinger H, Heydt C, et al. Implementation of amplicon parallel sequencing leads to improvement of diagnosis and therapy of lung cancer patients. J Thorac Oncol 2015;10:1049-57.
20. Sos ML, Michel K, Zander T,Weiss J, Frommolt P, Peifer M, et al. Predicting drug susceptibility of non-small cell lung cancers based on genetic lesions. J Clin Invest 2009;119:1727-40.
21. Peifer M, Weiss J, Sos ML, Koker M, Heynck S, Netzer C, et al. Analysis of compound synergy in high-throughput cellular screens by populationbased lifetime modeling. PLoS ONE 2010;5:e8919.
22. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 2000;92:205-16.
23. Takezawa K, Pirazzoli V, Arcila ME, Nebhan CA, Song X, de Stanchina E, et al. HER2 amplification: a potential mechanism of acquired resistance to EGFR inhibition in EGFR-mutant lung cancers that lack the second-site EGFRT790M mutation. Cancer Discov 2012;2: 922-33.
24. Wilson TR, Fridlyand J, Yan Y, Penuel E, Burton L, Chan E, et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012;487:505-9.
25. Planchard D, Loriot Y, André F, Gobert A, Auger N, Lacroix L, et al. EGFRindependent mechanisms of acquired resistance to AZD9291 in EGFR T790M-positive NSCLC patients. Ann Oncol 2015;26:2073-8.
26. Ercan D, Choi HG, Yun C-H, Capelletti M, Xie T, Eck MJ, et al. EGFR mutations and resistance to Irreversible pyrimidine based EGFR inhibitors. Clin Cancer Res 2015;21:3913-23
27. Niederst MJ, Hu H, Mulvey HE, Lockerman EL, Garcia AR, Piotrowska Z, et al. The allelic context of the C797S mutation acquired upon treatment with third generation EGFR inhibitors impacts sensitivity to subsequent treatmentstrategies. Clin Cancer Res 2015;21:3924-33.
28. Wong SQ, Li J, Tan AY-C, Vedururu R, Pang J-MB, Do H, et al. Sequence artefacts in a prospective series of formalin-fixed tumours tested for mutations in hotspot regions by massively parallel sequencing. BMC Med Genomics 2014;7:23.
29. Engelman J, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007;316:1039-43.
30. Turke AB, Zejnullahu K, Wu Y-L, Song Y, Dias-Santagata D, Lifshits E, et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010;17:77-88.
31. Bean J, Brennan C, Shih J-Y, 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.
32. Haringsma HJ, Allen A, Harding TC, Simmons AD. In vivo acquired resistance to the mutant EGFR inhibitor Rociletinib (CO-1686) is associated with activation of the c-MET pathway. Abstract 3595. doi: 10.1158/1538-7445.AM2015-3595 Published 1 August 2015. AACR 106th Annual Meeting 2015; April 18-22, 2015.
33. Scheffler M, Merkelbach-Bruse S, Bos M, Fassunke J, Gardizi M, Michels S, et al. Spatial tumor heterogeneity in lung cancer with acquired epidermal growth factor receptor-tyrosine kinase inhibitor resistance: targeting high-level MET-amplification and EGFR T790M mutation occurring at different sites in the same patient. J Thorac Oncol 2015; 10:e40-3.
34. Oxnard GR, Ramalingam SS, Ahn M-J, Kim S-W, Yu HA, Saka H, et al. Preliminary results of TATTON, a multi-arm phase Ib trial of AZD9291combined with MEDI4736, AZD6094 or selumetinib in EGFR-mutant lung cancer. J Clin Oncol 2015;33 (suppl; abstr 2509).
35. Pao W, Miller VA. Epidermal growth factor receptor mutations, smallmolecule kinase inhibitors, and non-small cell lung cancer: current knowledge and future directions. J Clin Oncol 2005;23:2556-68.
36. Gainor JF, Varghese AM, Ou S-HI, 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.
37. Choughule A, Sharma R, Trivedi V, Thavamani A, Noronha V, Joshi A, et al. Coexistence of KRAS mutation with mutant but not wild-type EGFR predicts response to tyrosine-kinase inhibitors in human lung cancer. Br J Cancer 2014;111:2203-4.
38. Hrustanovic G, Olivas V, Pazarentzos E, Tulpule A, Asthana S, Blakely CM, et al. RAS-MAPK dependence underlies a rational polytherapy strategy in EML4-ALK-positive lung cancer. Nat Med 2015;21:1038-47.
39. Cargnelutti M, Corso S, Pergolizzi M, Mévellec L, Aisner DL, Dziadziuszko R, et al. Activation of RAS family members confers resistance to ROS1 targeting drugs. Oncotarget 2015;6: 5182-94.
40. de Bruin EC, Cowell C, Warne PH, Jiang M, Saunders RE, Melnick MA, et al. Reduced NF1 expression confers resistance to EGFR inhibition in lung cancer. Cancer Discov 2014;4:606-19.
41. Suda K, Mizuuchi H, Murakami I, Uramoto H, Tanaka F, Sato K, et al. CRKL amplification is rare as a mechanism for acquired resistance to kinase inhibitors in lung cancers with epidermal growth factor receptor mutation. Lung Cancer 2014;85:147-51.
42. Suda K, Mizuuchi H, Sato K, Takemoto T, Iwasaki T, Mitsudomi T. The insulin-like growth factor 1 receptor causes acquired resistance to erlotinib in lung cancer cells with thewild-type epidermal growth factor receptor. Int J Cancer 2014;135:1002-6.
43. Piotrowska Z, Niederst MJ, Karlovich CA, Wakelee HA, Neal JW, Mino- Kenudson M, et al. Heterogeneity underlies the emergence of EGFR T790 wild-type clones following treatment of T790M-positive cancers with a third generation EGFR inhibitor. Cancer Discov 2015;5: 713-22.