Targeted next-generation sequencing of DNA regions proximal to a conserved GXGXXG signaling motif enables systematic discovery of tyrosine kinase fusions in cancer

Nucleic Acids Research

Volumn 38, Issue 20, 2010, Pages 6985-6996

  Chmielecki, Juliann ^a   Peifer, Martin ^b   Jia, Peilin ^c   Socci, Nicholas D ^d   Hutchinson, Katherine ^e   Viale, Agnes ^d   Zhao, Zhongming ^c   Thomas, Roman K ^b,f   Pao, William ^e  

^a Weill Cornell Graduate School of Biomedical Sciences   (United States)

^b UNIVERSITY OF COLOGNE   (Germany)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e VANDERBILT INGRAM CANCER CENTER   (United States)

^f CHEMICAL GENOMICS CENTRE OF THE MAX PLANCK SOCIETY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; ANAPLASTIC LYMPHOMA KINASE; B RAF KINASE; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; GENOMIC DNA; GLYCINE; JANUS KINASE 2; MESSENGER RNA; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN KINASE B; PROTEIN KINASE B BETA; PROTEIN RET; PROTEIN TYROSINE KINASE;

ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DNA DETERMINATION; DNA SEQUENCE; GENE FUSION; GENE MAPPING; GENETIC CONSERVATION; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; LEUKEMIA CELL; MALIGNANT NEOPLASTIC DISEASE; PRIORITY JOURNAL; PROTEIN MOTIF; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; THYROID CANCER;

AMINO ACID MOTIFS; CELL LINE, TUMOR; CHROMOSOME BREAKPOINTS; CHROMOSOME MAPPING; CONSERVED SEQUENCE; CYTOSKELETAL PROTEINS; HUMANS; MUTANT CHIMERIC PROTEINS; NEOPLASM PROTEINS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-RET; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, PROTEIN; SIGNAL TRANSDUCTION;

EID: 78651287445     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq579     Document Type: Article

References (38)

1. Sawyers, C. (2004) Targeted cancer therapy. Nature, 432, 294-297.
2. Druker, B. J. (2002) STI571 (Gleevec) as a paradigm for cancer therapy. Trends Mol. Med., 8, S14-18.
3. Hantschel, O., Nagar, B., Guettler, S., Kretzschmar, J., Dorey, K., Kuriyan, J. and Superti-Furga, G. (2003) A myristoyl/phosphotyrosine switch regulates c-Abl. Cell, 112, 845-857.
4. Nagar, B., Hantschel, O., Young, M. A., Scheffzek, K., Veach, D., Bornmann, W., Clarkson, B., Superti-Furga, G. and Kuriyan, J. (2003) Structural basis for the autoinhibition of c-Abl tyrosine kinase. Cell, 112, 859-871.
5. Kumar-Sinha, C., Tomlins, S. A. and Chinnaiyan, A. M. (2006) Evidence of recurrent gene fusions in common epithelial tumors. Trends Mol. Med., 12, 529-536.
6. Santoro, M., Rosati, R., Grieco, M., Berlingieri, M. T., D'Amato, G. L., de Franciscis, V. and Fusco, A. (1990) The ret proto-oncogene is consistently expressed in human pheochromocytomas and thyroid medullary carcinomas. Oncogene, 5, 1595-1598.
7. Ciampi, R., Knauf, J. A., Kerler, R., Gandhi, M., Zhu, Z., Nikiforova, M. N., Rabes, H. M., Fagin, J. A. and Nikiforov, Y. E. (2005) Oncogenic AKAP9-BRAF fusion is a novel mechanism of MAPK pathway activation in thyroid cancer. J. Clin. Invest., 115, 94-101.
8. Rabes, H. M., Demidchik, E. P., Sidorow, J. D., Lengfelder, E., Beimfohr, C., Hoelzel, D. and Klugbauer, S. (2000) Pattern of radiation-induced RET and NTRK1 rearrangements in 191 post-chernobyl papillary thyroid carcinomas: biological, phenotypic, and clinical implications. Clin. Cancer Res., 6, 1093-1103.
9. Rikova, K., Guo, A., Zeng, Q., Possemato, A., Yu, J., Haack, H., Nardone, J., Lee, K., Reeves, C., Li, Y. et al. (2007) Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell, 131, 1190-1203.
10. Soda, M., Choi, Y. L., Enomoto, M., Takada, S., Yamashita, Y., Ishikawa, S., Fujiwara, S., Watanabe, H., Kurashina, K., Hatanaka, H. et al. (2007) Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature, 448, 561-566.
11. Takeuchi, K., Choi, Y. L., Togashi, Y., Soda, M., Hatano, S., Inamura, K., Takada, S., Ueno, T., Yamashita, Y., Satoh, Y. et al. (2009) KIF5B-ALK, a novel fusion oncokinase identified by an immunohistochemistry-based diagnostic system for ALK-positive lung cancer. Clin. Cancer Res., 15, 3143-3149.
12. Horn, L. and Pao, W. (2009) EML4-ALK: Honing in on a new target in non-small-cell lung cancer. J. Clin. Oncol., 27, 4232-4235.
13. Maher, C. A., Kumar-Sinha, C., Cao, X., Kalyana-Sundaram, S., Han, B., Jing, X., Sam, L., Barrette, T., Palanisamy, N. and Chinnaiyan, A. M. (2009) Transcriptome sequencing to detect gene fusions in cancer. Nature, 458, 97-101.
14. Maher, C. A., Palanisamy, N., Brenner, J. C., Cao, X., Kalyana-Sundaram, S., Luo, S., Khrebtukova, I., Barrette, T. R., Grasso, C., Yu, J. et al. (2009) Chimeric transcript discovery by paired-end transcriptome sequencing. Proc. Natl Acad. Sci. USA, 106, 12353-12358.
15. Campbell, P. J., Stephens, P. J., Pleasance, E. D., O'Meara, S., Li, H., Santarius, T., Stebbings, L. A., Leroy, C., Edkins, S., Hardy, C. et al. (2008) Identification of somatically acquired rearrangements in cancer using genome-wide massively parallel paired-end sequencing. Nat. Genet., 40, 722-729.
16. Stephens, P. J., McBride, D. J., Lin, M. L., Varela, I., Pleasance, E. D., Simpson, J. T., Stebbings, L. A., Leroy, C., Edkins, S., Mudie, L. J. et al. (2009) Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature, 462, 1005-1010.
17. Zhao, Q., Caballero, O. L., Levy, S., Stevenson, B. J., Iseli, C., de Souza, S. J., Galante, P. A., Busam, D., Leversha, M. A., Chadalavada, K. et al. (2009) Transcriptome-guided characterization of genomic rearrangements in a breast cancer cell line. Proc. Natl Acad. Sci. USA, 106, 1886-1891.
18. Berger, M. F., Levin, J. Z., Vijayendran, K., Sivachenko, A., Adiconis, X., Maguire, J., Johnson, L. A., Robinson, J., Verhaak, R. G., Sougnez, C. et al. Integrative analysis of the melanoma transcriptome. Genome Res.
19. Leary, R. J., Kinde, I., Diehl, F., Schmidt, K., Clouser, C., Duncan, C., Antipova, A., Lee, C., McKernan, K., De La Vega, F. M. et al. (2010) Development of personalized tumor biomarkers using massively parallel sequencing. Science Translational Medicine, 2.
20. Levin, J. Z., Berger, M. F., Adiconis, X., Rogov, P., Melnikov, A., Fennell, T., Nusbaum, C., Garraway, L. A. and Gnirke, A. (2009) Targeted next-generation sequencing of a cancer transcriptome enhances detection of sequence variants and novel fusion transcripts. Genome Biol., 10, R115.
21. Albert, T. J., Molla, M. N., Muzny, D. M., Nazareth, L., Wheeler, D., Song, X., Richmond, T. A., Middle, C. M., Rodesch, M. J., Packard, C. J. et al. (2007) Direct selection of human genomic loci by microarray hybridization. Nat. Methods, 4, 903-905.
22. Gnirke, A., Melnikov, A., Maguire, J., Rogov, P., LeProust, E. M., Brockman, W., Fennell, T., Giannoukos, G., Fisher, S., Russ, C. et al. (2009) Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nat. Biotechnol., 27, 182-189.
23. Okou, D. T., Steinberg, K. M., Middle, C., Cutler, D. J., Albert, T. J. and Zwick, M. E. (2007) Microarray-based genomic selection for high-throughput resequencing. Nat. Methods, 4, 907-909.
24. Hodges, E., Xuan, Z., Balija, V., Kramer, M., Molla, M. N., Smith, S. W., Middle, C. M., Rodesch, M. J., Albert, T. J., Hannon, G. J. et al. (2007) Genome-wide in situ exon capture for selective resequencing. Nat. Genet., 39, 1522-1527.
25. Manning, G., Whyte, D. B., Martinez, R., Hunter, T. and Sudarsanam, S. (2002) The protein kinase complement of the human genome. Science, 298, 1912-1934.
26. Kent, W. J., Sugnet, C. W., Furey, T. S., Roskin, K. M., Pringle, T. H., Zahler, A. M. and Haussler, D. (2002) The human genome browser at UCSC. Genome Res, 12, 996-1006.
27. Jossart, G. H., Greulich, K. M., Siperstein, A. E., Duh, Q., Clark, O. H. and Weier, H. U. (1995) Molecular and cytogenetic characterization of a t (1;10;21) translocation in the human papillary thyroid cancer cell line TPC-1 expressing the ret/H4 chimeric transcript. Surgery, 118, 1018-1023.
28. Gu, T. L., Goss, V. L., Reeves, C., Popova, L., Nardone, J., Macneill, J., Walters, D. K., Wang, Y., Rush, J., Comb, M. J. et al. (2006) Phosphotyrosine profiling identifies the KG-1 cell line as a model for the study of FGFR1 fusions in acute myeloid leukemia. Blood, 108, 4202-4204.
29. Kent, W. J. (2002) BLAT-the BLAST-like alignment tool. Genome Res., 12, 656-664.
30. Hanks, S. K., Quinn, A. M. and Hunter, T. (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science, 241, 42-52.
31. Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J., Braverman, M. S., Chen, Y. J., Chen, Z. et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature, 437, 376-380.
32. Ciampi, R., Knauf, J. A., Rabes, H. M., Fagin, J. A. and Nikiforov, Y. E. (2005) BRAF kinase activation via chromosomal rearrangement in radiation-induced and sporadic thyroid cancer. Cell Cycle, 4, 547-548.
33. Bean, J., Brennan, C., Shih, J. Y., Riely, G., Viale, A., Wang, L., Chitale, D., Motoi, N., Szoke, J., Broderick, S. et al. (2007) MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib. Proc. Natl Acad. Sci. USA, 104, 20932-20937.
34. Tracy, S., Mukohara, T., Hansen, M., Meyerson, M., Johnson, B. E. and Janne, P. A. (2004) Gefitinib induces apoptosis in the EGFRL858R non-small-cell lung cancer cell line H3255. Cancer Res., 64, 7241-7244.
35. Nowell, P. C. and Hungerford, D. A. (1960) Chromosome studies on normal and leukemic human leukocytes. J. Natl Cancer Inst., 25, 85-109.
36. Rowley, J. D. (1973) Letter: a new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature, 243, 290-293.
37. Ben-Neriah, Y., Daley, G. Q., Mes-Masson, A. M., Witte, O. N. and Baltimore, D. (1986) The chronic myelogenous leukemia-specific P210 protein is the product of the bcr/abl hybrid gene. Science, 233, 212-214.
38. Koivunen, J. P., Mermel, C., Zejnullahu, K., Murphy, C., Lifshits, E., Holmes, A. J., Choi, H. G., Kim, J., Chiang, D., Thomas, R. et al. (2008) EML4-ALK fusion gene and efficacy of an ALK kinase inhibitor in lung cancer. Clin. Cancer Res., 14, 4275-4283.