Clinical utility of cell-free DNA for the detection of ALK fusions and genomic mechanisms of ALK inhibitor resistance in non–small cell lung cancer

Clinical Cancer Research

Volumn 24, Issue 12, 2018, Pages 2758-2770

  McCoach, Caroline E ^a   Blakely, Collin M ^a   Banks, Kimberly C ^b   Levy, Benjamin ^c   Chue, Ben M ^d   Raymond, Victoria M ^b   Le, Anh T ^e   Lee, Christine E ^b   Diaz, Joseph ^b   Waqar, Saiama N ^f   Purcell, William T ^e   Aisner, Dara L ^e   Davies, Kurtis D ^e   Lanman, Richard B ^b   Shaw, Alice T ^g   Doebele, Robert C ^e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Guardant Health   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d Lifespring Cancer Treatment Center   (United States)

^e UNIVERSITY OF COLORADO CANCER CENTER   (United States)

^f WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALECTINIB; ANAPLASTIC LYMPHOMA KINASE; BEVACIZUMAB; CERITINIB; CIRCULATING TUMOR DNA; CRIZOTINIB; ERLOTINIB; LORLATINIB; OSIMERTINIB; PEMBROLIZUMAB; POTASSIUM CHANNEL KCNQ; ANTINEOPLASTIC AGENT; CELL FREE NUCLEIC ACID; ONCOPROTEIN; PROTEIN KINASE INHIBITOR;

ADULT; AGED; ANAPLASTIC LYMPHOMA KINASE GENE; ARTICLE; CANCER RESISTANCE; COPY NUMBER VARIATION; DRUG SUBSTITUTION; DRUG WITHDRAWAL; EML4 GENE; FEMALE; GENE; GENE FUSION; GENOMICS; HUMAN; HUMAN TISSUE; KCNQ GENE; KIF5B GENE; KLC1 GENE; MAJOR CLINICAL STUDY; MALE; NEXT GENERATION SEQUENCING; NON SMALL CELL LUNG CANCER; PPM1B GENE; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SINGLE NUCLEOTIDE POLYMORPHISM; STRN GENE; TGF GENE; GENETICS; HIGH THROUGHPUT SEQUENCING; LUNG TUMOR; MIDDLE AGED; PROCEDURES; TUMOR CELL LINE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANAPLASTIC LYMPHOMA KINASE; ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL-FREE NUCLEIC ACIDS; FEMALE; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; LUNG NEOPLASMS; MALE; MIDDLE AGED; ONCOGENE PROTEINS, FUSION; PROTEIN KINASE INHIBITORS;

EID: 85051133542     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-17-2588     Document Type: Article

References (53)

1. Mok TS, Wu YL, Thongprasert S, Yang CH, Chu DT, Saijo N, et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009;361:947–57.
2. Mitsudomi T, Morita S, Yatabe Y, Negoro S, Okamoto I, Tsurutani J, et al. Gefitinib versus cisplatin plus docetaxel in patients with non-small-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol 2010;11:121–8.
3. Rosell R, Carcereny E, Gervais R, Vergnenegre A, Massuti B, Felip E, et al. Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre, open-label, randomised phase 3 trial. Lancet Oncol 2012;13:239–46.
4. 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.
5. Shaw AT, Yeap BY, Solomon BJ, Riely GJ, Gainor J, Engelman JA, et al. Effect of crizotinib on overall survival in patients with advanced non-small-cell lung cancer harbouring ALK gene rearrangement: a retrospective analysis. Lancet Oncol 2011;12:1004–12.
6. Camidge DR, Bang YJ, Kwak EL, Iafrate AJ, Varella-Garcia M, Fox SB, et al. Activity and safety of crizotinib in patients with ALK-positive non-small-cell lung cancer: updated results from a phase 1 study. Lancet Oncol 2012;13:1011–9.
7. Shaw AT, Kim DW, Nakagawa K, Seto T, Crino L, Ahn MJ, et al. Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N Engl J Med 2013;368:2385–94.
8. Solomon BJ, Mok T, Kim DW, Wu YL, Nakagawa K, Mekhail T, et al. First-line crizotinib versus chemotherapy in ALK-positive lung cancer. N Engl J Med 2014;371:2167–77.
9. Ettinger DS, Wood DE, Aisner DL, Akerley W, Bauman J, Chirieac LR, et al. Non-small cell lung cancer, version 5.2017, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 2017;15:504–35.
10. Gainor JF, Dardaei L, Yoda S, Friboulet L, Leshchiner I, Katayama R, et al. Molecular mechanisms of resistance to first- and second-generation ALK inhibitors in ALK-rearranged lung cancer. Cancer Discov 2016;6:1118–33.
11. Shaw AT, Friboulet L, Leshchiner I, Gainor JF, Bergqvist S, Brooun A, et al. Resensitization to crizotinib by the lorlatinib ALK resistance mutation L1198F. N Engl J Med 2016;374:54–61.
12. Meric-Bernstam F, Brusco L, Shaw K, Horombe C, Kopetz S, Davies MA, et al. Feasibility of large-scale genomic testing to facilitate enrollment onto genomically matched clinical trials. J Clin Oncol 2015;33:2753–62.
13. Piotrowska Z, Drapkin B, Engelman JA, Nagy RJ, Lanman RB, Sequist LV. Plasma T790M result alters treatment options in a previously T790 wild-type EGFR-mutant lung cancer. J Thorac Oncol 2016;11:e95–7.
14. Goyal L, Saha SK, Liu LY, Siravegna G, Leshchiner I, Ahronian LG, et al. Polyclonal secondary FGFR2 mutations drive acquired resistance to FGFR inhibition in patients with FGFR2 fusion-positive cholangiocarcinoma. Cancer Discov 2017;7:252–63.
15. Jamal-Hanjani M, Wilson GA, McGranahan N, Birkbak NJ, Watkins TBK, Veeriah S, et al. Tracking the evolution of non-small-cell lung cancer. N Engl J Med 2017;376:2109–21.
16. Lokhandwala T, Bittoni MA, Dann RA, D'Souza AO, Johnson M, Nagy RJ, et al. Costs of diagnostic assessment for lung cancer: a medicare claims analysis. Clin Lung Cancer 2017;18:e27–e34.
17. National Lung Screening Trial Research T, Aberle DR, Adams AM, Berg CD, Black WC, Clapp JD, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med 2011;365: 395–409.
18. Thompson JC, Yee SS, Troxel AB, Savitch SL, Fan R, Balli D, et al. Detection of therapeutically targetable driver and resistance mutations in lung cancer patients by next-generation sequencing of cell-free circulating tumor DNA. Clin Cancer Res 2016;22:5772–82.
19. Schwaederle M, Husain H, Fanta PT, Piccioni DE, Kesari S, Schwab RB, et al. Detection rate of actionable mutations in diverse cancers using a biopsy-free (blood) circulating tumor cell DNA assay. Oncotarget 2016;7: 9707–17.
20. Lanman RB, Mortimer SA, Zill OA, Sebisanovic D, Lopez R, Blau S, et al. Analytical and clinical validation of a digital sequencing panel for quantitative, highly accurate evaluation of cell-free circulating tumor DNA. PLoS One 2015;10:e0140712.
21. Villaflor V, Won B, Nagy R , Banks K, Lanman RB, Talasaz A,etal.Biopsy-free circulating tumor DNA assay identifies actionable mutations in lung cancer. Oncotarget 2016;7:66880–91.
22. Kim ST, Lee WS, Lanman RB, Mortimer S, Zill OA, Kim KM, et al. Prospective blinded study of somatic mutation detection in cell-free DNA utilizing a targeted 54-gene next generation sequencing panel in metastatic solid tumor patients. Oncotarget 2015;6:40360–9.
23. Paweletz CP, Sacher AG, Raymond CK, Alden RS, O'Connell A, Mach SL, et al. Bias-corrected targeted next-generation sequencing for rapid, multiplexed detection of actionable alterations in cell-free DNA from advanced lung cancer patients. Clin Cancer Res 2016;22: 915–22.
24. Jenkins S, Yang JC, Ramalingam SS, Yu K, Patel S, Weston S, et al. Plasma ctDNA analysis for detection of the EGFR T790M mutation in patients with advanced non-small cell lung cancer. J Thorac Oncol 2017;12:1061–70.
25. Cui S, Zhang W, Xiong L, Pan F, Niu Y, Chu T, et al. Use of capture-based next-generation sequencing to detect ALK fusion in plasma cell-free DNA of patients with non-small-cell lung cancer. Oncotarget 2017;8: 2771–80.
26. Bordi P, Tiseo M, Rofi E, Petrini I, Restante G, Danesi R, et al. Detection of ALK and KRAS mutations in circulating tumor DNA of patients with advanced ALK-positive NSCLC with disease progression during crizotinib treatment. Clin Lung Cancer 2017;18:692–7.
27. Dagogo-Jack I, Brannon AR, Ferris LA, Campbell CD, Lin JJ, Schultz KR, et al. Tracking the evolution of resistance to ALK tyrosine kinase inhibitors through longitudinal analysis of circulating tumor DNA. JCO Precis Oncol 2018:2018. doi: 10.1200/PO.17.00160. Epub 2018 Jan 23.
28. Vowles J, Odegaard J, Mortimer S, Fairclough S, Sikora M, Abdueva D, et al. Analytical validation of Guardant360 v2.10. Paper presented at: Annual Association for Cancer Research; April 5, 2017; Washington, DC.
29. Ding L, Getz G, Wheeler DA, Mardis ER, McLellan MD, Cibulskis K, et al. Somatic mutations affect key pathways in lung adenocarcinoma. Nature 2008;455:1069–75.
30. Govindan R, Ding L, Griffith M, Subramanian J, Dees ND, Kanchi KL, et al. Genomic landscape of non-small cell lung cancer in smokers and never-smokers. Cell 2012;150:1121–34.
31. Pilling AB, Kim J, Estrada-Bernal A, Zhou Q, Le AT, Singleton KR, et al. ALK is a critical regulator of the MYC-signaling axis in ALK positive lung cancer. Oncotarget 2018;9:8823–35.
32. Lin J, Zhu V, Yoda S, et al. MA 07.07 clinical outcomes and ALK resistance mutations in ALK+ non-small cell lung cancer according to EML4-ALK variant. J Thorac Oncol 12:S1828.
33. + non-small cell lung cancer (NSCLC). J Clin Oncol. 2017;35(15_suppl):9010.
34. Ali SM, Hensing T, Schrock AB, Allen J, Sanford E, Gowen K, et al. Comprehensive genomic profiling identifies a subset of crizotinib-responsive ALK-rearranged non-small cell lung cancer not detected by fluorescence in situ hybridization. Oncologist 2016;21:762–70.
35. Gainor JF, Shaw AT, Sequist LV, Fu X, Azzoli CG, Piotrowska Z, et al. EGFR mutations and ALK rearrangements are associated with low response rates to PD-1 pathway blockade in non-small cell lung cancer: a retrospective analysis. Clin Cancer Res 2016;22:4585–93.
36. Sarfaty M, Moore A, Neiman V, Dudnik E, Ilouze M, Gottfried M, et al. RET fusion lung carcinoma: response to therapy and clinical features in a case series of 14 patients. Clin Lung Cancer 2017;18:e223–32.
37. + non-small cell lung cancer. J Clin Oncol 34, 2016(suppl; abstr 9065).
38. + NSCLC patients. J Clin Oncol. 2012;30, 2012 (suppl; abstr 7504).
39. Liang W, He Q, Chen Y, Chuai S, Yin W, Wang W, et al. Metastatic EML4-ALK fusion detected by circulating DNA genotyping in an EGFR-mutated NSCLC patient and successful management by adding ALK inhibitors: a case report. BMC Cancer 2016;16:62.
40. Doebele RC, Pilling AB, Aisner DL, Kutateladze TG, Le AT, Weickhardt AJ, et al. Mechanisms of resistance to crizotinib in patients with ALK gene rearranged non-small cell lung cancer. Clin Cancer Res 2012;18: 1472–82.
41. Mack PC, Banks KC, Zill OA, Mortimer SA, Chudova DI, Odegaard J, et al. O.02: Plasma next generation sequencing of over 5,000 advanced non-small cell lung cancer patients with clinical correlations. J Thorac Oncol 2016;11:S168–9.
42. Kelly LM, Barila G, Liu P, Evdokimova VN, Trivedi S, Panebianco F, et al. Identification of the transforming STRN-ALK fusion as a potential therapeutic target in the aggressive forms of thyroid cancer. Proc Natl Acad Sci U S A 2014;111:4233–8.
43. Perot G, Soubeyran I, Ribeiro A, Bonhomme B, Savagner F, Boutet-Bou-zamondo N, et al. Identification of a recurrent STRN/ALK fusion in thyroid carcinomas. PLoS One 2014;9:e87170.
44. Nakanishi Y, Masuda S, Iida Y, Takahashi N, Hashimoto S. Case report of non-small cell lung cancer with STRN-ALK translocation: a nonresponder to alectinib. J Thorac Oncol 2017;12:e202–4.
45. Moqrich A, Mattei MG, Bartoli M, Rakitina T, Baillat G, Monneron A, et al. Cloning of human striatin cDNA (STRN), gene mapping to 2p22-p21, and preferential expression in brain. Genomics 1998;51:136–9.
46. Dietrich MF, Yan SX, Schiller JH. Response to crizotinib/erlotinib combination in a patient with a primary EGFR-mutant adenocarcinoma and a primary c-met-amplified adenocarcinoma of the lung. J Thorac Oncol 2015;10:e23–5.
47. Gainor JF, Niederst MJ, Lennerz JK, Dagogo-Jack I, Stevens S, Shaw AT, et al. Dramatic response to combination erlotinib and crizotinib in a patient with advanced, EGFR-mutant lung cancer harboring de novo MET amplification. J Thorac Oncol 2016;11:e83–5.
48. Ou SI, Govindan R, Eaton KD, Otterson GA, Gutierrez ME, Mita AC, et al. Phase I results from a study of crizotinib in combination with erlotinib in patients with advanced nonsquamous non-small cell lung cancer. J Thorac Oncol 2017;12:145–51.
49. Majewski IJ, Mittempergher L, Davidson NM, Bosma A, Willems SM, Horlings HM, et al. Identification of recurrent FGFR3 fusion genes in lung cancer through kinome-centred RNA sequencing. J Pathol 2013; 230:270–6.
50. Ou SI, Horn L, Cruz M, Vafai D, Lovly CM, Spradlin A, et al. Emergence of FGFR3-TACC3 fusions as a potential by-pass resistance mechanism to EGFR tyrosine kinase inhibitors in EGFR mutated NSCLC patients. Lung Cancer 2017;111:61–4.
51. Klempner SJ, Bazhenova LA, Braiteh FS, Nikolinakos PG, Gowen K, Cervantes CM, et al. Emergence of RET rearrangement co-existing with activated EGFR mutation in EGFR-mutated NSCLC patients who had progressed on first- or second-generation EGFR TKI. Lung Cancer 2015;89:357–9.
52. Allen JM, Schrock AB, Erlich RL, Miller VA, Stephens PJ, Ross JS, et al. Genomic profiling of circulating tumor DNA in relapsed EGFR-mutated lung adenocarcinoma reveals an acquired FGFR3-TACC3 fusion. Clin Lung Cancer 2017;18:e219–22.
53. Takeuchi K, Choi YL, Soda M, Inamura K, Togashi Y, Hatano S, et al. Multiplex reverse transcription-PCR screening for EML4-ALK fusion transcripts. Clin Cancer Res 2008;14:6618–24.