Targeted expression of mutated ALK induces neuroblastoma in transgenic mice

Science Translational Medicine

Volumn 4, Issue 141, 2012, Pages

  Heukamp, Lukas C ^a   Thor, Theresa ^b   Schramm, Alexander ^b   De Preter, Katleen ^c   Kumps, Candy ^c   De Wilde, Bram ^c   Odersky, Andrea ^b   Peifer, Martin ^d   Lindner, Sven ^b   Spruessel, Annika ^b   Pattyn, Filip ^c   Mestdagh, Pieter ^c   Menten, Björn ^c   Kuhfittig Kulle, Steffi ^b   Künkele, Annette ^b   König, Katharina ^a   Meder, Lydia ^a   Chatterjee, Sampurna ^d   Ullrich, Roland T ^d   Schulte, Stefanie ^b   Vandesompele, Jo ^c   Speleman, Frank ^c   Büttner, Reinhard ^a   Eggert, Angelika ^b   Schulte, Johannes H ^b   more..

^a UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

^c GHENT UNIVERSITY HOSPITAL   (Belgium)

^d UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; ENZYME INHIBITOR; TAE 684; UNCLASSIFIED DRUG; NVP TAE684; NVP-TAE684; PROTEIN TYROSINE KINASE; PYRIMIDINE DERIVATIVE;

ALK ONCOGENE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CHROMOSOME 17Q; CHROMOSOME ABERRATION; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVITY; GENE AMPLIFICATION; GENE EXPRESSION; GENE TARGETING; GENETIC GAIN; HUMAN; METASTASIS; MORPHOLOGY; MOUSE; MYCN ONCOGENE; NEURAL CREST; NEUROBLASTOMA; NEUROSECRETION; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECRETORY VESICLE; SYNAPSE; TRANSGENE; TRANSGENIC MOUSE; TUMOR REGRESSION; ANIMAL; GENETICS; METABOLISM;

ANIMALS; HUMANS; MICE; MICE, TRANSGENIC; NEUROBLASTOMA; PYRIMIDINES; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 84863569496     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3003967     Document Type: Article

References (24)

1. J. M. Maris, Recent advances in neuroblastoma. N. Engl. J. Med. 362, 2202-2211 (2010).
2. T. Iwahara, J. Fujimoto, D. Wen, R. Cupples, N. Bucay, T. Arakawa, S. Mori, B. Ratzkin, T. Yamamoto, Molecular characterization of ALK, a receptor tyrosine kinase expressed specifically in the nervous system. Oncogene 14, 439-449 (1997).
3. S. W. Morris, M. N. Kirstein, M. B. Valentine, K. G. Dittmer, D. N. Shapiro, D. L. Saltman, A. T. Look, Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma. Science 263, 1281-1284 (1994).
4. S. W. Morris, C. Naeve, P. Mathew, P. L. James, M. N. Kirstein, X. Cui, D. P. Witte, ALK, the chromosome 2 gene locus altered by the t(2;5) in non-Hodgkin's lymphoma, encodes a novel neural receptor tyrosine kinase that is highly related to leukocyte tyrosine kinase (LTK). Oncogene 14, 2175-2188 (1997).
5. M. Soda, Y. L. Choi, M. Enomoto, S. Takada, Y. Yamashita, S. Ishikawa, S. Fujiwara, H. Watanabe, K. Kurashina, H. Hatanaka, M. Bando, S. Ohno, Y. Ishikawa, H. Aburatani, T. Niki, Y. Sohara, Y. Sugiyama, H. Mano, Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 448, 561-566 (2007).
6. E. L. Kwak, Y. J. Bang, D. R. Camidge, A. T. Shaw, B. Solomon, R. G. Maki, S. H. Ou, B. J. Dezube, P.A. Jänne, D. B. Costa, M. Varella-Garcia, W. H. Kim, T. J. Lynch, P. Fidias, H. Stubbs, J. A. Engelman, L. V. Sequist, W. Tan, L. Gandhi, M. Mino-Kenudson, G. C. Wei, S. M. Shreeve, M. J. Ratain, J. Settleman, J. G. Christensen, D. A. Haber, K. Wilner, R. Salgia, G. I. Shapiro, J. W. Clark, A. J. Iafrate, Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N. Engl. J. Med. 363, 1693-1703 (2010).
7. Y. Chen, J. Takita, Y. L. Choi, M. Kato, M. Ohira, M. Sanada, L. Wang, M. Soda, A. Kikuchi, T. Igarashi, A. Nakagawara, Y. Hayashi, H. Mano, S. Ogawa, Oncogenic mutations of ALK kinase in neuroblastoma. Nature 455, 971-974 (2008).
8. R. E. George, T. Sanda, M. Hanna, S. Fröhling, W. Luther II, J. Zhang, Y. Ahn, W. Zhou, W. B. London, P. McGrady, L. Xue, S. Zozulya, V. E. Gregor, T. R. Webb, N. S. Gray, D. G. Gilliland, L. Diller, H. Greulich, S. W. Morris, M. Meyerson, A. T. Look, Activating mutations in ALK provide a therapeutic target in neuroblastoma. Nature 455, 975-978 (2008).
9. I. Janoueix-Lerosey, D. Lequin, L. Brugières, A. Ribeiro, L. de Pontual, V. Combaret, V. Raynal, A. Puisieux, G. Schleiermacher, G. Pierron, D. Valteau-Couanet, T. Frebourg, J. Michon, S. Lyonnet, J. Amiel, O. Delattre, Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma. Nature 455, 967-970 (2008).
10. Y. P. Mossé, M. Laudenslager, L. Longo, K. A. Cole, A. Wood, E. F. Attiyeh, M. J. Laquaglia, R. Sennett, J. E. Lynch, P. Perri, G. Laureys, F. Speleman, C. Kim, C. Hou, H. Hakonarson, A. Torkamani, N. J. Schork, G. M. Brodeur, G. P. Tonini, E. Rappaport, M. Devoto, J. M. Maris, Identification of ALK as a major familial neuroblastoma predisposition gene. Nature 455, 930-935 (2008).
11. S. De Brouwer, K. De Preter, C. Kumps, P. Zabrocki, M. Porcu, E. M. Westerhout, A. Lakeman, J. Vandesompele, J. Hoebeeck, T. Van Maerken, A. De Paepe, G. Laureys, J. H. Schulte, A. Schramm, C. Van Den Broecke, J. Vermeulen, N. Van Roy, K. Beiske, M. Renard, R. Noguera, O. Delattre, I. Janoueix-Lerosey, P. Kogner, T. Martinsson, A. Nakagawara, M. Ohira, H. Caron, A. Eggert, J. Cools, R. Versteeg, F. Speleman, Meta-analysis of neuroblastomas reveals a skewed ALK mutation spectrum in tumors with MYCN amplification. Clin. Cancer Res. 16, 4353-4362 (2010).
12. T. Sasaki, K. Okuda, W. Zheng, J. Butrynski, M. Capelletti, L. Wang, N. S. Gray, K. Wilner, J. G. Christensen, G. Demetri, G. I. Shapiro, S. J. Rodig, M. J. Eck, P. A. Jänne, The neuroblastoma-associated F1174L ALKmutation causes resistance to an ALK kinase inhibitor in ALK-translocated cancers. Cancer Res. 70, 10038-10043 (2010).
13. J. Maurer, S. Fuchs, R. Jäger, B. Kurz, L. Sommer, H. Schorle, Establishment and controlled differentiation of neural crest stem cell lines using conditional transgenesis. Differentiation 75, 580-591 (2007).
14. M. Stanke, C. V. Duong, M. Pape, M. Geissen, G. Burbach, T. Deller, H. Gascan, C.Otto, R. Parlato, G. Schutz, H. Rohrer, Target-dependent specification of the neurotransmitter phenotype: Cholinergic differentiation of sympathetic neurons is mediated in vivo by gp130 signaling. Development 133, 141-150 (2006).
15. J. Lindeberg, D. Usoskin, H. Bengtsson, A. Gustafsson, A. Kylberg, S. Söderström, T. Ebendal, Transgenic expression of Cre recombinase from the tyrosine hydroxylase locus. Genesis 40, 67-73 (2004).
16. W. A. Weiss, K. Aldape, G. Mohapatra, B. G. Feuerstein, J. M. Bishop, Targeted expression of MYCN causes neuroblastoma in transgenic mice. EMBO J. 16, 2985-2995 (1997).
17. G. Schleiermacher, I. Janoueix-Lerosey, A. Ribeiro, J. Klijanienko, J. Couturier, G. Pierron, V. Mosseri, A. Valent, N. Auger, D. Plantaz, H. Rubie, D. Valteau-Couanet, F. Bourdeaut, V. Combaret, C. Bergeron, J. Michon, O. Delattre, Accumulation of segmental alterations determines progression in neuroblastoma. J. Clin. Oncol. 28, 3122-3130 (2010).
18. C. S. Hackett, J. G. Hodgson, M. E. Law, J. Fridlyand, K. Osoegawa, P. J. de Jong, N. J. Nowak, D. Pinkel, D. G. Albertson, A. Jain, R. Jenkins, J. W. Gray, W. A. Weiss, Genome-wide array CGH analysis of murine neuroblastoma reveals distinct genomic aberrations which parallel those in human tumors. Cancer Res. 63, 5266-5273 (2003).
19. S. C. Bresler, A. C. Wood, E. A. Haglund, J. Courtright, L. T. Belcastro, J. S. Plegaria, K. Cole, Y. Toporovskaya, H. Zhao, E. L. Carpenter, J. G. Christensen, J. M. Maris, M. A. Lemmon, Y. P. Mossé, Differential inhibitor sensitivity of anaplastic lymphoma kinase variants found in neuroblastoma. Sci. Transl. Med. 3, 108ra114 (2011).
20. C. Schönherr, K. Ruuth, S. Kamaraj, C. L. Wang, H. L. Yang, V. Combaret, A. Djos, T. Martinsson, J. G. Christensen, R. H. Palmer, B. Hallberg, Anaplastic lymphoma kinase (ALK) regulates initiation of transcription of MYCN in neuroblastoma cells. Oncogene 10.1038/onc.2012.12 (2012).
21. I. Varela, C. Klijn, P. J. Stephens, L. J. Mudie, L. Stebbings, D. Galappaththige, H. van der Gulden, E. Schut, S. Klarenbeek, P. J. Campbell, L. F. Wessels, M. R. Stratton, J. Jonkers, P. A. Futreal, D. J. Adams, Somatic structural rearrangements in genetically engineered mouse mammary tumors. Genome Biol. 11, R100 (2010).
22. R. Meuwissen, S. C. Linn, M. van der Valk, W. J. Mooi, A. Berns, Mouse model for lung tumorigenesis through Cre/lox controlled sporadic activation of the K-Ras oncogene. Oncogene 20, 6551-6558 (2001).
23. E. Fredlund, M. Ringnér, J. M. Maris, S. Påhlman, High Myc pathway activity and low stage of neuronal differentiation associate with poor outcome in neuroblastoma. Proc. Natl. Acad. Sci. U.S.A. 105, 14094-14099 (2008).
24. J. H. Schulte, H. S. Bachmann, B. Brockmeyer, K. Depreter, A. Oberthur, S. Ackermann, Y. Kahlert, K. Pajtler, J. Theissen, F. Westermann, J. Vandesompele, F. Speleman, F. Berthold, A. Eggert, B. Brors, B. Hero, A. Schramm, M. Fischer, High ALK receptor tyrosine kinase expression supersedes ALK mutation as a determining factor of an unfavorable phenotype in primary neuroblastoma. Clin. Cancer Res. 17, 5082-5092 (2011).