Fusion of EML4 and ALK is associated with development of lung adenocarcinomas lacking EGFR and KRAS mutations and is correlated with ALK expression

Molecular Cancer

Volumn 9, Issue , 2010, Pages

  Zhang, Xuchao ^a   Zhang, Shirley ^a   Yang, Xuening ^a   Yang, Jinji ^a   Zhou, Qing ^a   Yin, Lucy ^a   An, Shejuan ^a   Lin, Jiaying ^a   Chen, Shiliang ^a   Xie, Zhi ^a   Zhu, Mike ^a   Zhang, Xiaolin ^a   Wu, Yi long ^a  

^a GUANGDONG PROVINCIAL PEOPLE'S HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; EML4 ALK FUSION PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; HYBRID PROTEIN; K RAS PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG; EML4 ALK FUSION PROTEIN, HUMAN; EML4-ALK FUSION PROTEIN, HUMAN; ONCOPROTEIN;

ADULT; ARTICLE; CANCER SURVIVAL; CHINESE; CONTROLLED STUDY; CORRELATIONAL STUDY; FEMALE; FUSION GENE; GENE EXPRESSION; GENE FREQUENCY; GENE IDENTIFICATION; GENE MUTATION; GENETIC ASSOCIATION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; LUNG ADENOCARCINOMA; LUNG NON SMALL CELL CANCER; MALE; MUTATIONAL ANALYSIS; ONSET AGE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ADENOCARCINOMA; COHORT ANALYSIS; GENETICS; LUNG TUMOR; MUTATION; NUCLEOTIDE SEQUENCE; ONCOGENE RAS; PATHOLOGY; TUMOR CELL LINE;

ADENOCARCINOMA; BASE SEQUENCE; CELL LINE, TUMOR; COHORT STUDIES; GENES, RAS; HUMANS; LUNG NEOPLASMS; MUTATION; ONCOGENE PROTEINS, FUSION; RECEPTOR, EPIDERMAL GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 77954399760     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-9-188     Document Type: Article

References (40)

1. Morris SW, Kirstein MN, Valentine MB, Dittmer KG, Shapiro DN, Saltman DL, Look AT. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma. Science 1994, 263:1281-1284. 10.1126/science.8122112, 8122112.
2. Palmer RH, Vernersson E, Grabbe C, Hallberg B. Anaplastic lymphoma kinase: signalling in development and disease. Biochemical Journal 2009, 420:345-361. 10.1042/BJ20090387, 2708929, 19459784.
3. Polgar D, Leisser C, Maier S, Strasser S, Ruger B, Dettke M, Khorchide M, Simonitsch I, Cerni C, Krupitza G. Truncated ALK derived from chromosomal translocation t(2;5)(p23;q35) binds to the SH3 domain of p85-PI3K. Mutation Research 2005, 570:9-15.
4. Coffin CM, Hornick JL, Fletcher CD. Inflammatory myofibroblastic tumor: comparison of clinicopathologic, histologic, and immunohistochemical features including ALK expression in atypical and aggressive cases. American Journal of Surgical Pathology 2007, 31:509-520. 10.1097/01.pas.0000213393.57322.c7, 17414097.
5. Chen Y, Takita J, Choi YL, Kato M, Ohira M, Sanada M, Wang L, Soda M, Kikuchi A, Igarashi T, et al. Oncogenic mutations of ALK kinase in neuroblastoma. Nature 2008, 455:971-974. 10.1038/nature07399, 18923524.
6. George RE, Sanda T, Hanna M, Frohling S, Luther W, Zhang J, Ahn Y, Zhou W, London WB, McGrady P, et al. Activating mutations in ALK provide a therapeutic target in neuroblastoma. Nature 2008, 455:975-978. 10.1038/nature07397, 2587486, 18923525.
7. Janoueix-Lerosey I, Lequin D, Brugieres L, Ribeiro A, de Pontual L, Combaret V, Raynal V, Puisieux A, Schleiermacher G, Pierron G, et al. Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma.[see comment]. Nature 2008, 455:967-970. 10.1038/nature07398, 18923523.
8. Soda M, Choi YL, Enomoto M, Takada S, Yamashita Y, Ishikawa S, Fujiwara S, Watanabe H, Kurashina K, Hatanaka H, et al. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer.[see comment]. Nature 2007, 448:561-566. 10.1038/nature05945, 17625570.
9. Tort F, Campo E, Pohlman B, Hsi E. Heterogeneity of genomic breakpoints in MSN-ALK translocations in anaplastic large cell lymphoma. Human Pathology 2004, 35:1038-1041. 10.1016/j.humpath.2004.05.006, 15297972.
10. Kinoshita Y, Tajiri T, Ieiri S, Nagata K, Taguchi T, Suita S, Yamazaki K, Yoshino I, Maehara Y, Kohashi K, et al. A case of an inflammatory myofibroblastic tumor in the lung which expressed TPM3-ALK gene fusion. Pediatric Surgery International 2007, 23:595-599. 10.1007/s00383-006-1821-6, 17063337.
11. Armstrong F, Lamant L, Hieblot C, Delsol G, Touriol C. TPM3-ALK expression induces changes in cytoskeleton organisation and confers higher metastatic capacities than other ALK fusion proteins. European Journal of Cancer 2007, 43:640-646. 10.1016/j.ejca.2006.12.005, 17276053.
12. Ma Z, Cools J, Marynen P, Cui X, Siebert R, Gesk S, Schlegelberger B, Peeters B, De Wolf-Peeters C, Wlodarska I, Morris SW. Inv(2)(p23q35) in anaplastic large-cell lymphoma induces constitutive anaplastic lymphoma kinase (ALK) tyrosine kinase activation by fusion to ATIC, an enzyme involved in purine nucleotide biosynthesis. Blood 2000, 95:2144-2149.
13. Trinei M, Lanfrancone L, Campo E, Pulford K, Mason DY, Pelicci PG, Falini B. A new variant anaplastic lymphoma kinase (ALK)-fusion protein (ATIC-ALK) in a case of ALK-positive anaplastic large cell lymphoma. Cancer Research 2000, 60:793-798.
14. Colleoni GW, Bridge JA, Garicochea B, Liu J, Filippa DA, Ladanyi M. ATIC-ALK: A novel variant ALK gene fusion in anaplastic large cell lymphoma resulting from the recurrent cryptic chromosomal inversion, inv(2)(p23q35). American Journal of Pathology 2000, 156:781-789. 1876849, 10702393.
15. Hernandez L, Pinyol M, Hernandez S, Bea S, Pulford K, Rosenwald A, Lamant L, Falini B, Ott G, Mason DY, et al. TRK-fused gene (TFG) is a new partner of ALK in anaplastic large cell lymphoma producing two structurally different TFG-ALK translocations. Blood 1999, 94:3265-3268.
16. Cools J, Wlodarska I, Somers R, Mentens N, Pedeutour F, Maes B, De Wolf-Peeters C, Pauwels P, Hagemeijer A, Marynen P. Identification of novel fusion partners of ALK, the anaplastic lymphoma kinase, in anaplastic large-cell lymphoma and inflammatory myofibroblastic tumor. Genes, Chromosomes & Cancer 2002, 34:354-362.
17. Touriol C, Greenland C, Lamant L, Pulford K, Bernard F, Rousset T, Mason DY, Delsol G. Further demonstration of the diversity of chromosomal changes involving 2p23 in ALK-positive lymphoma: 2 cases expressing ALK kinase fused to CLTCL (clathrin chain polypeptide-like). Blood 2000, 95:3204-3207.
18. Takeuchi K, Choi YL, Togashi Y, Soda M, Hatano S, Inamura K, Takada S, Ueno T, Yamashita Y, Satoh Y, et al. KIF5B-ALK, a novel fusion oncokinase identified by an immunohistochemistry-based diagnostic system for ALK-positive lung cancer. Clinical Cancer Research 2009, 15:3143-3149. 10.1158/1078-0432.CCR-08-3248, 19383809.
19. Mano H. Non-solid oncogenes in solid tumors: EML4-ALK fusion genes in lung cancer. Cancer Science 2008, 99:2349-2355. 10.1111/j.1349-7006.2008.00972.x, 19032370.
20. Pollmann M, Parwaresch R, Adam-Klages S, Kruse ML, Buck F, Heidebrecht HJ. Human EML4, a novel member of the EMAP family, is essential for microtubule formation. Experimental Cell Research 2006, 312:3241-3251. 10.1016/j.yexcr.2006.06.035, 16890222.
21. Houtman SH, Rutteman M, De Zeeuw CI, French PJ. Echinoderm microtubule-associated protein like protein 4, a member of the echinoderm microtubule-associated protein family, stabilizes microtubules. Neuroscience 2007, 144:1373-1382. 10.1016/j.neuroscience.2006.11.015, 17196341.
22. Rikova K, Guo A, Zeng Q, Possemato A, Yu J, Haack H, Nardone J, Lee K, Reeves C, Li Y, et al. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 2007, 131:1190-1203. 10.1016/j.cell.2007.11.025, 18083107.
23. Horn L, Pao W. EML4-ALK: honing in on a new target in non-small-cell lung cancer.[comment]. Journal of Clinical Oncology 2009, 27:4232-4235. 10.1200/JCO.2009.23.6661, 19667260.
24. Soda M, Takada S, Takeuchi K, Choi YL, Enomoto M, Ueno T, Haruta H, Hamada T, Yamashita Y, Ishikawa Y, et al. A mouse model for EML4-ALK-positive lung cancer. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:19893-19897. 10.1073/pnas.0805381105, 2605003, 19064915.
25. Kwak EL, Camidge DR, Clark J, Shapiro GI, Maki RG, Ratain MJ, Solomon B, Bang Y, Ou S, Salgia R. Clinical activity observed in a phase I dose escalation trial of an oral c- met and ALK inhibitor, PF-02341066. Journal of Clinical Oncology 2009, 27:15s. (suppl; abstr 3509):15s.
26. Bang Y, Kwak EL, Shaw AT, Camidge DR, Iafrate AJ, Maki RG, Solomon BJ, Ou SI, Salgia R, Clark JW. Clinical activity of the oral ALK inhibitor PF-02341066 in ALK-positive patients with non-small cell lung cancer (NSCLC). Journal of Clinical Oncology 2010, 28:7s. (suppl; abstr 3):7s.
27. Solomon B, Varella-Garcia M, Camidge DR. ALK gene rearrangements: a new therapeutic target in a molecularly defined subset of non-small cell lung cancer. Journal of Thoracic Oncology: Official Publication of the International Association for the Study of Lung Cancer 2009, 4:1450-1454.
28. Tan LH, Do E, Chong SM, Koay ES. Detection of ALK gene rearrangements in formalin-fixed, paraffin-embedded tissue using a fluorescence in situ hybridization (FISH) probe: a search for optimum conditions of tissue archiving and preparation for FISH. Molecular Diagnosis 2003, 7:27-33. 10.2165/00066982-200307010-00005, 14529317.
29. Takeuchi K, Choi YL, Soda M, Inamura K, Togashi Y, Hatano S, Enomoto M, Takada S, Yamashita Y, Satoh Y, et al. Multiplex reverse transcription-PCR screening for EML4-ALK fusion transcripts. Clinical Cancer Research 2008, 14:6618-6624. 10.1158/1078-0432.CCR-08-1018, 18927303.
30. Koivunen JP, Mermel C, Zejnullahu K, Murphy C, Lifshits E, Holmes AJ, Choi HG, Kim J, Chiang D, Thomas R, et al. EML4-ALK fusion gene and efficacy of an ALK kinase inhibitor in lung cancer. Clinical Cancer Research 2008, 14:4275-4283. 10.1158/1078-0432.CCR-08-0168, 18594010.
31. Perner S, Wagner PL, Demichelis F, Mehra R, Lafargue CJ, Moss BJ, Arbogast S, Soltermann A, Weder W, Giordano TJ, et al. EML4-ALK fusion lung cancer: a rare acquired event. Neoplasia (New York) 2008, 10:298-302.
32. Wong DW, Leung EL, So KK, Tam IY, Sihoe AD, Cheng LC, Ho KK, Au JS, Chung LP, Pik Wong M, . University of Hong Kong Lung Cancer Study G 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. 10.1002/cncr.24181, 19170230, University of Hong Kong Lung Cancer Study G.
33. Martelli MP, Sozzi G, Hernandez L, Pettirossi V, Navarro A, Conte D, Gasparini P, Perrone F, Modena P, Pastorino U, et al. EML4-ALK rearrangement in non-small cell lung cancer and non-tumor lung tissues. American Journal of Pathology 2009, 174:661-670. 10.2353/ajpath.2009.080755, 2630573, 19147828.
34. Shaw AT, Yeap BY, Mino-Kenudson M, Digumarthy SR, Costa DB, Heist RS, Solomon B, Stubbs H, Admane S, McDermott U, et al. Clinical features and outcome of patients with non-small-cell lung cancer who harbor EML4-ALK.[see comment]. Journal of Clinical Oncology 2009, 27:4247-4253. 10.1200/JCO.2009.22.6993, 19667264.
35. Inamura K, Takeuchi K, Togashi Y, Hatano S, Ninomiya H, Motoi N, Mun MY, Sakao Y, Okumura S, Nakagawa K, et al. EML4-ALK lung cancers are characterized by rare other mutations, a TTF-1 cell lineage, an acinar histology, and young onset. Modern Pathology 2009, 22:508-515. 10.1038/modpathol.2009.2, 19234440.
36. Shinmura K, Kageyama S, Tao H, Bunai T, Suzuki M, Kamo T, Takamochi K, Suzuki K, Tanahashi M, Niwa H, et al. EML4-ALK fusion transcripts, but no NPM-, TPM3-, CLTC-, ATIC-, or TFG-ALK fusion transcripts, in non-small cell lung carcinomas. Lung Cancer 2008, 61:163-169. 10.1016/j.lungcan.2007.12.013, 18242762.
37. Inamura K, Takeuchi K, Togashi Y, Nomura K, Ninomiya H, Okui M, Satoh Y, Okumura S, Nakagawa K, Soda M, et al. EML4-ALK fusion is linked to histological characteristics in a subset of lung cancers. Journal of Thoracic Oncology: Official Publication of the International Association for the Study of Lung Cancer 2008, 3:13-17.
38. Choi YL, Takeuchi K, Soda M, Inamura K, Togashi Y, Hatano S, Enomoto M, Hamada T, Haruta H, Watanabe H, et al. Identification of novel isoforms of the EML4-ALK transforming gene in non-small cell lung cancer. Cancer Research 2008, 68:4971-4976. 10.1158/0008-5472.CAN-07-6158, 18593892.
39. Boland JM, Erdogan S, Vasmatzis G, Yang P, Tillmans LS, Johnson MR, Wang X, Peterson LM, Halling KC, Oliveira AM, et al. Anaplastic lymphoma kinase immunoreactivity correlates with ALK gene rearrangement and transcriptional up-regulation in non-small cell lung carcinomas. Human Pathology 2009, 40:1152-1158. 10.1016/j.humpath.2009.01.012, 19386350.
40. Jiang SX, Yamashita K, Yamamoto M, Piao CJ, Umezawa A, Saegusa M, Yoshida T, Katagiri M, Masuda N, Hayakawa K, Okayasu I. EGFR genetic heterogeneity of nonsmall cell lung cancers contributing to acquired gefitinib resistance. International Journal of Cancer 2008, 123:2480-2486.