Large-scale screening and molecular characterization of EML4-ALK fusion variants in archival non-small-cell lung cancer tumor specimens using quantitative reverse transcription polymerase chain reaction assays

Journal of Thoracic Oncology

Volumn 9, Issue 1, 2014, Pages 18-25

  Li, Tianhong ^a,b   Maus, Martin K H ^c,d   Desai, Sonal J ^a,b   Beckett, Laurel A ^a,e   Stephens, Craig ^d   Huang, Eric ^d   Hsiang, Jack ^d   Zeger, Gary ^d,f   Danenberg, Kathleen D ^d   Astrow, Stephanie H ^d   Gandara, David R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF COLOGNE   (Germany)

^d Response Genetics Inc ^*  (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Echinoderm microtubule associated protein like 4 anaplastic lymphoma kinase fusion variants; Formalin fixed; Non small cell lung cancer; Paraffinembedded; Quantitative; Reverse transcription polymerase chain reaction

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; EPIDERMAL GROWTH FACTOR RECEPTOR; HYBRID PROTEIN; K RAS PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 4; THYMIDYLATE SYNTHASE;

ADENOSQUAMOUS CARCINOMA; ADULT; AGED; ARTICLE; CANCER PATIENT; COMPARATIVE STUDY; CONTROLLED STUDY; ECHINODERM; EXON; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENOTYPE; HUMAN; HUMAN TISSUE; LARGE CELL CARCINOMA; LUNG ADENOCARCINOMA; LUNG NON SMALL CELL CANCER; LUNG SQUAMOUS CELL CARCINOMA; MALE; MIDDLE AGED; MULTIPLEX POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN FUSION; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCREENING; TISSUE SECTION; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; CARCINOMA, NON-SMALL-CELL LUNG; FEMALE; GENOTYPE; HUMANS; LUNG NEOPLASMS; MALE; MIDDLE AGED; ONCOGENE PROTEINS, FUSION; PARAFFIN EMBEDDING; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84891819982     PISSN: 15560864     EISSN: 15561380     Source Type: Journal    
DOI: 10.1097/JTO.0000000000000030     Document Type: Article

References (51)

1. Morris SW, Kirstein MN, Valentine MB, et al. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkins lymphoma. Science 1994;263:1281-1284
2. Shiota M, Fujimoto J, Semba T, Satoh H, Yamamoto T, Mori S. Hyperphosphorylation of a novel 80 kDa protein-tyrosine kinase similar to Ltk in a human Ki-1 lymphoma cell line, AMS3. Oncogene 1994;9:1567-1574
3. Griffin CA, Hawkins AL, Dvorak C, Henkle C, Ellingham T, Perlman EJ. Recurrent involvement of 2p23 in inflammatory myofibroblastic tumors. Cancer Res 1999;59:2776-2780
4. Soda M, Choi YL, Enomoto M, et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 2007;448:561-566
5. Mossé YP, Laudenslager M, Longo L, et al. Identification of ALK as a major familial neuroblastoma predisposition gene. Nature 2008;455:930-935
6. Robertson FM, et al. Gene amplification of anaplastic lymphoma kinase in inflammatory breast cancer. Mol Cancer Ther 2011;10(11):Abst PR-4 2011
7. Lin E, Li L, Guan Y, et al. Exon array profiling detects EML4-ALK fusion in breast, colorectal, and non-small cell lung cancers. Mol Cancer Res 2009;7:1466-1476
8. Chiarle R, Voena C, Ambrogio C, Piva R, Inghirami G. The anaplastic lymphoma kinase in the pathogenesis of cancer. Nat Rev Cancer 2008;8:11-23
9. Soda M, Takada S, Takeuchi K, et al. A mouse model for EML4-ALKpositive lung cancer. Proc Natl Acad Sci U S A 2008;105:19893-19897
10. Koivunen JP, Mermel C, Zejnullahu K, et al. EML4-ALK fusion gene and efficacy of an ALK kinase inhibitor in lung cancer. Clin Cancer Res 2008;14:4275-4283
11. Takeuchi K, Choi YL, Soda M, et al. Multiplex reverse transcription- PCR screening for EML4-ALK fusion transcripts. Clin Cancer Res 2008;14:6618-6624
12. Choi YL, Takeuchi K, Soda M, et al. Identification of novel isoforms of the EML4-ALK transforming gene in non-small cell lung cancer. Cancer Res 2008;68:4971-4976
13. Wong DW, Leung EL, So KK, et al.; University of Hong Kong Lung Cancer Study Group. The EML4-ALK fusion gene is involved in various histologic types of lung cancers from nonsmokers with wild-type EGFR and KRAS. Cancer 2009;115:1723-1733
14. Maus MKH, Stephens C, Zeger G, Grimminger PP, Huang E. Identification of novel variant of EML4-ALK fusion gene in NSCLC: Potential benefits of the RT-PCR method. Internat J Biomed Sc 2012;8(1):1-6
15. Takeuchi K, Choi YL, Togashi Y, et al. KIF5B-ALK, a novel fusion oncokinase identified by an immunohistochemistry-based diagnostic system for ALK-positive lung cancer. Clin Cancer Res 2009;15:3143-3149
16. Rikova K, Guo A, Zeng Q, et al. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007;131:1190-1203
17. Togashi Y, Soda M, Sakata S, et al. KLC1-ALK: A novel fusion in lung cancer identified using a formalin-fixed paraffin-embedded tissue only. PLoS One 2012;7:e31323
18. Jung Y, Kim P, Jung Y, et al. Discovery of ALK-PTPN3 gene fusion from human non-small cell lung carcinoma cell line using next generation RNA sequencing. Genes Chromosomes Cancer 2012;51:590-597
19. Christensen JG, Zou HY, Arango ME, et al. Cytoreductive antitumor activity of PF-2341066, a novel inhibitor of anaplastic lymphoma kinase and c-Met, in experimental models of anaplastic large-cell lymphoma. Mol Cancer Ther 2007;6(12 Pt 1):3314-3322
20. Bergethon K, Shaw AT, Ou SH, et al. ROS1 rearrangements define a unique molecular class of lung cancers. J Clin Oncol 2012;30:863-870
21. Kwak EL, Bang YJ, Camidge DR, et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med 2010;363:1693-1703
22. Crino L, Kim D, Riely GJ, et al. Initial phase II results with crizotinib in advanced ALK-positive non-small cell lung cancer (NSCLC): PROFILE 1005. ASCO Meeting Abstracts 2011; 29(15):7514
23. Kim, D-W, Ahn M-J, Shi Y, et al. Results of a global phase II study with crizotinib in advanced ALK-positive non-small cell lung cancer (NSCLC). ASCO Meeting Abstracts 2012; 30(15):7533
24. Camidge DR, Bang YJ, Kwak EL, 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;13:1011-1019
25. Shaw AT, Yeap BY, Solomon BJ, 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;12:1004-1012
26. Danenberg PV, Stephens C, Cooc J, et al. A novel RT-PCR approach to detecting EML4-ALK fusion genes in archival NSCLC tissue. ASCO Meeting Abstracts 2010: 28(15):10535
27. Makino H, Uetake H, Danenberg K, Danenberg PV, Sugihara K. Efficacy of laser capture microdissection plus RT-PCR technique in analyzing gene expression levels in human gastric cancer and colon cancer. BMC Cancer 2008;8:210
28. Li T, Mack PC, Desai S, et al. Large-scale screening of ALK fusion oncogene transcripts in archival NSCLC tumor specimens using multiplexed RT-PCR assays. ASCO Meeting Abstracts 2011; 29(15):10520
29. Li T, Huang E, Desai S, et al. Update on the large-scale screening of ALK fusion oncogene transcripts in archival NSCLC tumor specimens using multiplexed RT-PCR assays. ASCO Meeting Abstracts 2012; 30(15):7594
30. Scagliotti GV, Parikh P, von Pawel J, et al. Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy- naive patients with advanced-stage non-small-cell lung cancer. J Clin Oncol 2008;26:3543-3551
31. Maus MK, Mack PC, Astrow SH, et al. Histology-related associations of ERCC1, RRM1, and TS biomarkers in patients with non-small-cell lung cancer: Implications for therapy. J Thorac Oncol 2013;8:582-586
32. Gandara DR, Huang E, Desai S, et al. Thymidylate synthase (TS) gene expression in patients with ALK positive (+) non-small cell lung cancer (NSCLC): Implications for therapy. ASCO Meeting Abstracts 2012; 30(15):7582
33. Camidge DR, Kono SA, Flacco A, et al. Optimizing the detection of lung cancer patients harboring anaplastic lymphoma kinase (ALK) gene rearrangements potentially suitable for ALK inhibitor treatment. Clin Cancer Res 2010;16:5581-5590
34. Zhang X, Zhang S, Yang X, et al. Fusion of EML4 and ALK is associated with development of lung adenocarcinomas lacking EGFR and KRAS mutations and is correlated with ALK expression. Mol Cancer 2010;9:188
35. Sasaki T, Jänne PA. New strategies for treatment of ALK-rearranged nonsmall cell lung cancers. Clin Cancer Res 2011;17:7213-7218
36. Wang Z, Zhang X, Bai H, et al. EML4-ALK rearrangement and its clinical significance in Chinese patients with advanced non-small cell lung cancer. Oncology 2012;83:248-256
37. Toyokawa G, Taguchi K, Ohba T, et al. First case of combined small-cell lung cancer with adenocarcinoma harboring EML4-ALK fusion and an exon 19 EGFR mutation in each histological component. J Thorac Oncol 2012;7:e39-e41
38. Sasaki T, Koivunen J, Ogino A, et al. A novel ALK secondary mutation and EGFR signaling cause resistance to ALK kinase inhibitors. Cancer Res 2011;71:6051-6060
39. Doebele RC, Pilling AB, Aisner DL, et al. Mechanisms of resistance to crizotinib in patients with ALK gene rearranged non-small cell lung cancer. Clin Cancer Res 2012;18:1472-1482
40. Li T, Kung HJ, Mack PC, Gandara DR. Genotyping and genomic profiling of non-small-cell lung cancer: Implications for current and future therapies. J Clin Oncol 2013;31:1039-1049
41. Keedy VL, Temin S, Somerfield MR, et al. American Society of Clinical Oncology provisional clinical opinion: Epidermal growth factor receptor (EGFR) Mutation testing for patients with advanced non-small-cell lung cancer considering first-line EGFR tyrosine kinase inhibitor therapy. J Clin Oncol 2011;29:2121-2127
42. Non-Small Cell Lung Cancer. Version 3.2012. NCCN Clinical Practice Guidelines in Oncology. Available at: Www.nccn.com. Accessed on May 25
43. Heuckmann JM, Balke-Want H, Malchers F, et al. Differential protein stability and ALK inhibitor sensitivity of EML4-ALK fusion variants. Clin Cancer Res 2012;18:4682-4690
44. Camidge, DR, Kono SA, Lu X, et al. Anaplastic lymphoma kinase gene rearrangements in non-small cell lung cancer are associated with prolonged progression-free survival on pemetrexed. J Thorac Oncol 2011;6(4):774-780
45. Lee JO, Kim TM, Lee SH, et al. Anaplastic lymphoma kinase translocation; a predictive biomarker of pemetrexed in patients with non-small cell lung cancer. J Thorac Oncol 2011;6:1474-1480
46. Shaw AT, Kim DW, Nakagawa K, et al. Phase III study of crizotinib vs pemetrexed or docetaxel chemotherapy in patients with advanced ALK-positive NSCLC (PROFILE 1007). ESMO 37th Annual Meeting 2012;Abst 2682, 2012
47. Shaw AT, Varghese AM, Solomon BJ, et al. Pemetrexed-based chemotherapy in patients with advanced, ALK-positive non-small cell lung cancer. Ann Oncol 2013;24:59-66
48. Choi YL, Soda M, Yamashita Y, et al.; ALK Lung Cancer Study Group. EML4-ALK mutations in lung cancer that confer resistance to ALK inhibitors. N Engl J Med 2010;363:1734-1739
49. Radich JP. How I monitor residual disease in chronic myeloid leukemia. Blood 2009;114:3376-3381
50. Wang R, Pan Y, Li C, et al. The use of quantitative real-time reverse transcriptase PCR for 5 and 3 portions of ALK transcripts to detect ALK rearrangements in lung cancers. Clin Cancer Res 2012;18:4725-4732
51. Soda M, Isobe K, Inoue A, et al.; North-East Japan Study Group; ALK Lung Cancer Study Group. A prospective PCR-based screening for the EML4-ALK oncogene in non-small cell lung cancer. Clin Cancer Res 2012;18:5682-5689