The frequency and clinical implication of ROS1 and RET rearrangements in resected stage IIIA-N2 non-small cell lung cancer patients

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Fu, Sha ^a   Liang, Ying ^a   Lin, Yong Bin ^a   Wang, Fang ^a   Huang, Ma Yan ^a   Zhang, Zi Chen ^a   Wang, Jing ^a   Cen, Wen Jian ^a   Shao, Jian Yong ^a  

^a SUN YAT SEN UNIVERSITY CANCER CENTER   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; ONCOPROTEIN; PROTEIN RET; PROTEIN TYROSINE KINASE; RET PROTEIN, HUMAN; ROS1 PROTEIN, HUMAN;

ACINAR CELL; ADULT; AGED; ARTICLE; CANCER PATIENT; CANCER RADIOTHERAPY; CANCER STAGING; CANCER SURVIVAL; CONTROLLED STUDY; EXON; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE FREQUENCY; GENE REARRANGEMENT; GENE SEQUENCE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG ADENOCARCINOMA; LUNG LOBECTOMY; LUNG RESECTION; LYMPH NODE DISSECTION; MAJOR CLINICAL STUDY; MALE; MEDIASTINUM LYMPH NODE; NON SMALL CELL LUNG CANCER; OVERALL SURVIVAL; POSTOPERATIVE CARE; PROGNOSIS; RET GENE; RETROSPECTIVE STUDY; ROS1 GENE; TISSUE MICROARRAY; TUMOR DIFFERENTIATION; TUMOR GENE; TUMOR INVASION; TUMOR LOCALIZATION; TUMOR VOLUME; CARCINOMA, NON-SMALL-CELL LUNG; GENETICS; LUNG NEOPLASMS; MIDDLE AGED;

AGED; CARCINOMA, NON-SMALL-CELL LUNG; FEMALE; GENE REARRANGEMENT; HUMANS; LUNG NEOPLASMS; MALE; MIDDLE AGED; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-RET; RETROSPECTIVE STUDIES;

EID: 84928409331     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0124354     Document Type: Article

References (50)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011; 61: 69-90. doi: 10.3322/caac.20107 PMID: 21296855
2. Mountain CF. Revisions in the International System for Staging Lung Cancer. Chest. 1997; 111: 1710-1717. PMID: 9187198
3. Tanaka F, Yanagihara K, Otake Y, Miyahara R, Kawano Y, Nakagawa T, et al. Surgery for non-small cell lung cancer: postoperative survival based on the revised tumor-node-metastasis classification and its time trend. Eur J Cardiothorac Surg. 2000; 18: 147-155. PMID: 10925222
4. Veeramachaneni NK, Feins RH, Stephenson BJ, Edwards LJ, Fernandez FG. Management of stage IIIA non-small cell lung cancer by thoracic surgeons in North America. Ann Thorac Surg. 2012; 94: 922-926. doi: 10.1016/j.athoracsur.2012.04.087 PMID: 22742842
5. Stinchcombe TE, Fried D, Morris DE, Socinski MA. Combined modality therapy for stage III non-small cell lung cancer. Oncologist. 2006; 11: 809-823. PMID: 16880240
6. Ichinose Y, Kato H, Koike T, Tsuchiya R, Fujisawa T, Shimizu N, et al. Overall survival and local recurrence of 406 completely resected stage IIIa-N2 non-small cell lung cancer patients: questionnaire survey of the Japan Clinical Oncology Group to plan for clinical trials. Lung Cancer. 2001; 34: 29-36. PMID: 11557110
7. Bergethon K, Shaw AT, Ou SH, Katayama R, Lovly CM, McDonald NT, et al. ROS1 rearrangements define a unique molecular class of lung cancers. J Clin Oncol. 2012; 30: 863-870. doi: 10.1200/JCO.2011.35.6345 PMID: 22215748
8. Shigematsu H, Lin L, Takahashi T, Nomura M, Suzuki M, Wistuba II, et al. Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancers. J Natl Cancer Inst. 2005; 97: 339-346. PMID: 15741570
9. Riely GJ, Politi KA, Miller VA, Pao W. Update on epidermal growth factor receptor mutations in non-small cell lung cancer. Clin Cancer Res. 2006; 12: 7232-7241. PMID: 17189394
10. Sequist LV, Bell DW, Lynch TJ, Haber DA. Molecular predictors of response to epidermal growth factor receptor antagonists in non-small-cell lung cancer. J Clin Oncol. 2007; 25: 587-595. PMID: 17290067
11. Horn L, Pao W. EML4-ALK: honing in on a new target in non-small-cell lung cancer. J Clin Oncol. 2009; 27: 4232-4235. doi: 10.1200/JCO.2009.23.6661 PMID: 19667260
12. Inamura K, Takeuchi K, Togashi Y, Hatano S, Ninomiya H, Motoi N, et al. EML4-ALK lung cancers are characterized by rare other mutations, a TTF-1 cell lineage, an acinar histology, and young onset. Mod Pathol. 2009; 22: 508-515. doi: 10.1038/modpathol.2009.2 PMID: 19234440
13. Shaw AT, Yeap BY, Mino-Kenudson M, Digumarthy SR, Costa DB, Heist RS, et al. Clinical features and outcome of patients with non-small-cell lung cancer who harbor EML4-ALK. J Clin Oncol. 2009; 27: 4247-4253. doi: 10.1200/JCO.2009.22.6993 PMID: 19667264
14. Kwak EL, Bang YJ, Camidge DR, Shaw AT, Solomon B, Maki RG, et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med. 2010; 363: 1693-1703. doi: 10.1056/NEJMoa1006448 PMID: 20979469
15. Esfahani K, Agulnik JS, Cohen V. A Systemic Review of Resistance Mechanisms and Ongoing Clinical Trials in ALK-Rearranged Non-Small Cell Lung Cancer. Front Oncol. 2014; 4: 174. doi: 10.3389/fonc.2014.00174 PMID: 25101240
16. Friboulet L, Li N, Katayama R, Lee CC, Gainor JF, Crystal AS, et al. The ALK inhibitor ceritinib overcomes crizotinib resistance in non-small cell lung cancer. Cancer Discov. 2014; 4: 662-673. doi: 10.1158/2159-8290.CD-13-0846 PMID: 24675041
17. Shen L, Ji HF. Ceritinib in ALK-rearranged non-small-cell lung cancer. N Engl J Med. 2014; 370: 2537. doi: 10.1056/NEJMc1404894#SA1 PMID: 24963576
18. Davies KD, Le AT, Theodoro MF, Skokan MC, Aisner DL, Berge EM, et al. Identifying and targeting ROS1 gene fusions in non-small cell lung cancer. Clin Cancer Res. 2012; 18: 4570-4579. doi: 10.1158/1078-0432.CCR-12-0550 PMID: 22919003
19. 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: 1121-1134. doi: 10.1016/j.cell.2012.08.024 PMID: 22980976
20. Ju YS, Lee WC, Shin JY, Lee S, Bleazard T, Won JK, et al. A transforming KIF5B and RET gene fusion in lung adenocarcinoma revealed from whole-genome and transcriptome sequencing. Genome Res. 2012; 22: 436-445. doi: 10.1101/gr.133645.111 PMID: 22194472
21. Kohno T, Ichikawa H, Totoki Y, Yasuda K, Hiramoto M, Nammo T, et al. KIF5B-RET fusions in lung adenocarcinoma. Nat Med. 2012; 18: 375-377. doi: 10.1038/nm.2644 PMID: 22327624
22. Rimkunas VM, Crosby KE, Li D, Hu Y, Kelly ME, Gu TL, et al. Analysis of receptor tyrosine kinase ROS1-positive tumors in non-small cell lung cancer: identification of a FIG-ROS1 fusion. Clin Cancer Res. 2012; 18: 4449-4457. doi: 10.1158/1078-0432.CCR-11-3351 PMID: 22661537
23. Seo JS, Ju YS, Lee WC, Shin JY, Lee JK, Bleazard T, et al. The transcriptional landscape and mutational profile of lung adenocarcinoma. Genome Res. 2012; 22: 2109-2119. doi: 10.1101/gr.145144.112 PMID: 22975805
24. Takeuchi K, Soda M, Togashi Y, Suzuki R, Sakata S, Hatano S, et al. RET, ROS1 and ALK fusions in lung cancer. Nat Med. 2012; 18: 378-381. doi: 10.1038/nm.2658 PMID: 22327623
25. Birchmeier C, O'Neill K, Riggs M, Wigler M. Characterization of ROS1 cDNA from a human glioblastoma cell line. Proc Natl Acad Sci U S A. 1990; 87: 4799-4803. PMID: 2352949
26. Sariola H, Saarma M. Novel functions and signalling pathways for GDNF. J Cell Sci. 2003; 116: 3855-3862. PMID: 12953054
27. Asai N, Jijiwa M, Enomoto A, Kawai K, Maeda K, Ichiahara M, et al. RET receptor signaling: dysfunction in thyroid cancer and Hirschsprung's disease. Pathol Int. 2006; 56: 164-172. PMID: 16634961
28. Wang X. Structural studies of GDNF family ligands with their receptors-Insights into ligand recognition and activation of receptor tyrosine kinase RET. Biochim Biophys Acta. 2013; 1834: 2205-2212. doi: 10.1016/j.bbapap.2012.10.008 PMID: 23085183
29. Gerber DE, Gandhi L, Costa DB. Management and future directions in non-small cell lung cancer with known activating mutations. Am Soc Clin Oncol Educ Book. 2014: e353-365. doi: 10.14694/EdBook-AM.2014.34.e353 PMID: 24857124
30. Drilon A, Wang L, Hasanovic A, Suehara Y, Lipson D, Stephens P, et al. Response to Cabozantinib in patients with RET fusion-positive lung adenocarcinomas. Cancer Discov. 2013; 3: 630-635. doi: 10.1158/2159-8290.CD-13-0035 PMID: 23533264
31. Cai W, Li X, Su C, Fan L, Zheng L, Fei K, et al. ROS1 fusions in Chinese patients with non-small-cell lung cancer. Ann Oncol. 2013; 24: 1822-1827. doi: 10.1093/annonc/mdt071 PMID: 23514723
32. Zhu ZH, Sun BY, Ma Y, Shao JY, Long H, Zhang X, et al. Three immunomarker support vector machines-based prognostic classifiers for stage IB non-small-cell lung cancer. J Clin Oncol. 2009; 27: 1091-1099. doi: 10.1200/JCO.2008.16.6991 PMID: 19188679
33. Tuononen K, Sarhadi VK, Wirtanen A, Ronty M, Salmenkivi K, Knuuttila A, et al. Targeted Resequencing Reveals ALK Fusions in Non-Small Cell Lung Carcinomas Detected by FISH, Immunohistochemistry, and Real-Time RT-PCR: A Comparison of Four Methods. Biomed Res Int. 2013; 2013: 757490. doi: 10.1155/2013/757490 PMID: 23484153
34. Zhang YG, Jin ML, Li L, Zhao HY, Zeng X, Jiang L, et al. Evaluation of ALK Rearrangement in Chinese Non-Small Cell Lung Cancer Using FISH, Immunohistochemistry, and Real-Time Quantitative RTPCR on Paraffin-Embedded Tissues. PLoS One. 2013; 8: e64821. doi: 10.1371/journal.pone.0064821 PMID: 23741400
35. Koivunen JP, Mermel C, Zejnullahu K, Murphy C, Lifshits E, Holmes AJ, et al. EML4-ALK fusion gene and efficacy of an ALK kinase inhibitor in lung cancer. Clin Cancer Res. 2008; 14: 4275-4283. doi: 10.1158/1078-0432.CCR-08-0168 PMID: 18594010
36. Camidge DR, Kono SA, Flacco A, Tan AC, Doebele RC, Zhou Q, 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. doi: 10.1158/1078-0432.CCR-10-0851 PMID: 21062932
37. Ou SH, Soo RA, Kubo A, Kawaguchi T, Ahn MJ. Will the Requirement by the US FDA to Simultaneously Co-Develop Companion Diagnostics (CDx) Delay the Approval of Receptor Tyrosine Kinase Inhibitors for RTK-Rearranged (ROS1-, RET-, AXL-, PDGFR-alpha-, NTRK1-) Non-Small Cell Lung Cancer Globally? Front Oncol. 2014; 4: 58. doi: 10.3389/fonc.2014.00058 PMID: 24744988
38. Pao W, Hutchinson KE. Chipping away at the lung cancer genome. Nat Med. 2012; 18: 349-351. doi: 10.1038/nm.2697 PMID: 22395697
39. Pan Y, Zhang Y, Li Y, Hu H, Wang L, Li H, et al. ALK, ROS1 and RET fusions in 1139 lung adenocarcinomas: a comprehensive study of common and fusion pattern-specific clinicopathologic, histologic and cytologic features. Lung Cancer. 2014; 84: 121-126. doi: 10.1016/j.lungcan.2014.02.007 PMID: 24629636
40. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature. 2007; 448: 561-566. PMID: 17625570
41. Perner S, Wagner PL, Demichelis F, Mehra R, Lafargue CJ, Moss BJ, et al. EML4-ALK fusion lung cancer: a rare acquired event. Neoplasia. 2008; 10: 298-302. PMID: 18320074
42. 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: 6618-6624. doi: 10.1158/1078-0432.CCR-08-1018 PMID: 18927303
43. Li C, Fang R, Sun Y, Han X, Li F, Gao B, et al. Spectrum of oncogenic driver mutations in lung adenocarcinomas from East Asian never smokers. PLoS One. 2011; 6: e28204. doi: 10.1371/journal.pone.0028204 PMID: 22140546
44. Cha YJ, Lee JS, Kim HR, Lim SM, Cho BC, Lee CY, et al. Screening of ROS1 rearrangements in lung adenocarcinoma by immunohistochemistry and comparison with ALK rearrangements. PLoS One. 2014; 9: e103333. doi: 10.1371/journal.pone.0103333 PMID: 25058391
45. Giovino GA, Mirza SA, Samet JM, Gupta PC, Jarvis MJ, Bhala N, et al. Tobacco use in 3 billion individuals from 16 countries: an analysis of nationally representative cross-sectional household surveys. Lancet. 2012; 380: 668-679. doi: 10.1016/S0140-6736(12)61085-X PMID: 22901888
46. Yoshida A, Tsuta K, Nakamura H, Kohno T, Takahashi F, Asamura H, et al. Comprehensive histologic analysis of ALK-rearranged lung carcinomas. Am J Surg Pathol. 2011; 35: 1226-1234. doi: 10.1097/PAS.0b013e3182233e06 PMID: 21753699
47. Yoshida A, Kohno T, Tsuta K, Wakai S, Arai Y, Shimada Y, et al. ROS1-rearranged lung cancer: a clinicopathologic and molecular study of 15 surgical cases. Am J Surg Pathol. 2013; 37: 554-562. doi: 10.1097/PAS.0b013e3182758fe6 PMID: 23426121
48. Chin LP, Soo RA, Soong R, Ou SH. Targeting ROS1 with anaplastic lymphoma kinase inhibitors: a promising therapeutic strategy for a newly defined molecular subset of non-small-cell lung cancer. J Thorac Oncol. 2012; 7: 1625-1630. doi: 10.1097/JTO.0b013e31826baf83 PMID: 23070242
49. Shaw AT, Camidge DR, Engelman JA, Solomon BJ, Kwak EL, Clark JW, et al. Clinical activity of crizotinib in advanced non-small cell lung cancer (NSCLC) harboring ROS1 gene rearrangement. J Clin Oncol. 2012; 30: (suppl) abstr 7508.
50. Lee HJ, Seol HS, Kim JY, Chun SM, Suh YA, Park YS, et al. ROS1 receptor tyrosine kinase, a druggable target, is frequently overexpressed in non-small cell lung carcinomas via genetic and epigenetic mechanisms. Ann Surg Oncol. 2013; 20: 200-208. doi: 10.1245/s10434-012-2553-6 PMID: 22915320