Anaplastic lymphoma kinase (ALK): Structure, oncogenic activation, and pharmacological inhibition

Pharmacological Research

Volumn 68, Issue 1, 2013, Pages 68-94

  Roskoski, Robert ^a  

^a Blue Ridge Institute for Medical Research   (United States)

Author keywords

Acquired drug resistance; Crizotinib; Drug discovery; Non small cell lung cancer; Protein kinase inhibitor; Targeted cancer therapy

Indexed keywords

5 (2,6 DICHLOROBENZYLSULFONYL) 3 [3,5 DIMETHYL 4 [2 (1 PYRROLIDINYLMETHYL) 1 PYRROLIDINYLCARBONYL] 1H PYRROL 2 YLMETHYLENE] 1,3 DIHYDRO 2H INDOL 2 ONE; AMGEN DERIVATIVE; ANAPLASTIC LYMPHOMA KINASE; AP 26113; ASP 3026; BENZIMIDAZOLE DERIVATIVE; BEVACIZUMAB; CARBAZOLE DERIVATIVE; CARBOPLATIN; CEP 28122; CEPHALON DERIVATIVE; CH 5424802; CH 5424842; CRIZOTINIB; CYCLOPHOSPHAMIDE; DOXORUBICIN; ERLOTINIB; GEFITINIB; GSK 1838705; LDK 378; PACLITAXEL; PREDNISONE; PROTEIN KINASE INHIBITOR; PYRIMIDINE DERIVATIVE; RITUXIMAB; TANESPIMYCIN; TRIAZINE DERIVATIVE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VINCRISTINE; X 396;

ADVANCED CANCER; ANAPLASTIC THYROID CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER RADIOTHERAPY; CANCER RESISTANCE; CANCER SURGERY; CANCER SURVIVAL; CARBOXY TERMINAL SEQUENCE; CHROMOSOME TRANSLOCATION; DOSE RESPONSE; DRUG BRAIN LEVEL; DRUG EFFICACY; DRUG PROTEIN BINDING; DRUG SAFETY; DRUG STRUCTURE; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME KINETICS; ENZYME PHOSPHORYLATION; ENZYME STRUCTURE; FATIGUE; GASTROINTESTINAL SYMPTOM; GENE OVEREXPRESSION; HUMAN; LARGE CELL LYMPHOMA; LIPOPHILICITY; LIVER TOXICITY; LUNG ADENOCARCINOMA; LUNG CANCER; LUNG NON SMALL CELL CANCER; LYMPHOCYTOPENIA; METASTASIS; NEUROBLASTOMA; NEUROPATHY; NEUTROPENIA; NONHUMAN; NUCLEOTIDE SEQUENCE; OVERALL SURVIVAL; PLASMA CELL GRANULOMA; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; RHABDOMYOSARCOMA; SIDE EFFECT; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; WEIGHT REDUCTION;

EID: 84872288990     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2012.11.007     Document Type: Review

References (165)

1. G. Manning, D.B. Whyte, R. Martinez, T. Hunter, and S. Sudarsanam The protein kinase complement of the human genome Science 298 2002 1912 1934
2. A. Alonso, J. Sasin, N. Bottini, I. Friedberg, I. Friedberg, and A. Osterman Protein tyrosine phosphatases in the human genome Cell 117 2004 699 711
3. R. Roskoski Jr. ERK1/2 MAP kinases: structure, function, and regulation Pharmacological Research 66 2012 105 143
4. S.S. Taylor, M.M. Keshwani, J.M. Steichen, and A.P. Kornev Evolution of the eukaryotic protein kinases as dynamic molecular switches Philosophical Transactions of the Royal Society London Biological Science 367 2012 2517 2528
5. A.E. Aleshin, M. Malfois, X. Liu, C.S. Kim, H.J. Fromm, and R.B. Honzatko Nonaggregating mutant of recombinant human hexokinase I exhibits wild-type kinetics and rod-like conformations in solution Biochemistry 38 1999 8359 8366
6. A. Fujioka, K. Terai, R.E. Itoh, K. Aoki, T. Nakamura, and S. Kuroda Dynamics of the Ras/ERK MAPK cascade as monitored by fluorescent probes Journal of Biological Chemistry 281 2006 8917 8926
7. B.D. Grant, and J.A. Adams Pre-steady-state kinetic analysis of cAMP-dependent protein kinase using rapid quench flow techniques Biochemistry 35 1996 2022 2029
8. M.A. Lemmon, and J. Schlessinger Cell signaling by receptor tyrosine kinases Cell 141 2010 1117 1134
9. S.W. Morris, M.N. Kirstein, M.B. Valentine, K. Dittmer, D.N. Shapiro, and A.T. Look Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma Science 267 1995 316 317
10. M. Shiota, J. Fujimoto, T. Semba, H. Satoh, T. Yamamoto, and S. Mori Hyperphosphorylation of a novel 80 kDa protein-tyrosine kinase similar to Ltk in a human Ki-1 lymphoma cell line, AMS3 Oncogene 9 1994 1567 1574
11. M. Soda, Y.L. Choi, M. Enomoto, S. Takada, Y. Yamashita, and S. Ishikawa Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer Nature 448 2007 561 566
12. K. Rikova, A. Guo, Q. Zeng, A. Possemato, J. Yu, and H. Haack Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer Cell 131 2007 1190 1203
13. F. Tabbó, A. Barreca, R. Piva, G. Inghirami European T-Cell Lymphoma Study Group ALK signaling and target therapy in anaplastic large cell lymphoma Frontiers in Oncology 2 2012 41
14. Y. Chen, J. Takita, Y.L. Choi, M. Kato, M. Ohira, and M. Sanada Oncogenic mutations of ALK kinase in neuroblastoma Nature 455 2008 971 974
15. R.E. George, T. Sanda, M. Hanna, S. Fröhling, W. Luther 2nd, and J. Zhang Activating mutations in ALK provide a therapeutic target in neuroblastoma Nature 455 2008 975 978
16. I. Janoueix-Lerosey, D. Lequin, L. Brugières, A. Ribeiro, L. de Pontual, and V. Combaret Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma Nature 455 2008 967 970
17. Y.P. Mossé, M. Laudenslager, L. Longo, K.A. Cole, A. Wood, and E.F. Attiyeh Identification of ALK as a major familial neuroblastoma predisposition gene Nature 455 2008 930 935
18. S.W. Morris, C. Naeve, P. Mathew, P.L. James, M.N. Kirstein, and X. Cui 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 1997 2175 2188 Erratum in: Oncogene 1997;15:2883
19. H. Mano ALKoma: a cancer subtype with a shared target Cancer Discovery 2 2012 495 502
20. C.E. Lorén, C. Englund, C. Grabbe, B. Hallberg, T. Hunter, and R.H. Palmer A crucial role for the anaplastic lymphoma kinase receptor tyrosine kinase in gut development in Drosophila melanogaster EMBO Reports 4 2003 781 786
21. G.E. Stoica, A. Kuo, A. Aigner, I. Sunitha, B. Souttou, and C. Malerczyk Identification of anaplastic lymphoma kinase as a receptor for the growth factor pleiotrophin Journal of Biological Chemistry 276 2001 16772 16779
22. G.E. Stoica, A. Kuo, C. Powers, E.T. Bowden, E.B. Sale, and A.T. Riegel Midkine binds to anaplastic lymphoma kinase (ALK) and acts as a growth factor for different cell types Journal of Biological Chemistry 277 2002 35990 35998
23. A. Motegi, J. Fujimoto, M. Kotani, H. Sakuraba, and T. Yamamoto ALK receptor tyrosine kinase promotes cell growth and neurite outgrowth Journal of Cell Science 117 2004 3319 3329
24. C. Moog-Lutz, J. Degoutin, J.Y. Gouzi, Y. Frobert, N. Brunet-de Carvalho, and J. Bureau Activation and inhibition of anaplastic lymphoma kinase receptor tyrosine kinase by monoclonal antibodies and absence of agonist activity of pleiotrophin Journal of Biological Chemistry 280 2005 26039 26048
25. T. Iwahara, J. Fujimoto, D. Wen, R. Cupples, N. Bucay, and T. Arakawa Molecular characterization of ALK, a receptor tyrosine kinase expressed specifically in the nervous system Oncogene 14 1997 439 449
26. E. Vernersson, N.K. Khoo, M.L. Henriksson, G. Roos, R.H. Palmer, and B. Hallberg Characterization of the expression of the ALK receptor tyrosine kinase in mice Gene Expression Patterns 6 2006 448 461
27. J.G. Bilsland, A. Wheeldon, A. Mead, P. Znamenskiy, S. Almond, and K.A. Waters Behavioral and neurochemical alterations in mice deficient in anaplastic lymphoma kinase suggest therapeutic potential for psychiatric indications Neuropsychopharmacology 33 2008 685 700
28. A.W. Lasek, J. Lim, C.L. Kliethermes, K.H. Berger, G. Joslyn, and G. Brush An evolutionary conserved role for anaplastic lymphoma kinase in behavioral responses to ethanol PLoS One 6 7 2011 e22636
29. D.R. Knighton, J.H. Zheng, L.F. Ten Eyck, V.A. Ashford, N.H. Xuong, and S.S. Taylor Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase Science 253 1991 407 414
30. S.S. Taylor, and A.P. Kornev Protein kinases: evolution of dynamic regulatory proteins Trends in Biochemical Sciences 36 2011 65 77
31. C.C. Lee, Y. Jia, N. Li, X. Sun, K. Ng, and E. Ambing Crystal structure of the ALK (anaplastic lymphoma kinase) catalytic domain Biochemical Journal 430 2010 425 437
32. R.T. Bossi, M.B. Saccardo, E. Ardini, M. Menichincheri, L. Rusconi, and P. Magnaghi Crystal structures of anaplastic lymphoma kinase in complex with ATP competitive inhibitors Biochemistry 49 2010 6813 6825
33. S.K. Hanks, A.M. Quinn, and T. Hunter The protein kinase family: conserved features and deduced phylogeny of the catalytic domains Science 241 1988 42 52
34. A.P. Kornev, N.M. Haste, S.S. Taylor, and L.F. Eyck Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism Proceedings of the National Academy of Sciences of the United States of America 103 2006 17783 17788
35. J. Zhou, and J.A. Adams Participation of ADP dissociation in the rate-determining step in cAMP-dependent protein kinase Biochemistry 36 1997 15733 15738
36. P.A. Schwartz, and B.W. Murray Protein kinase biochemistry and drug discovery Bioorganic Chemistry 39 2011 192 210
37. A.P. Kornev, and S.S. Taylor Defining the conserved internal architecture of a protein kinase Biochimica et Biophysica Acta 1804 2010 440 444
38. J. Zhang, P.L. Yang, and N.S. Gray Targeting cancer with small molecule kinase inhibitors Nature Reviews Cancer 9 2009 28 39
39. S.R. Hubbard, L. Wei, L. Ellis, and W.A. Hendrickson Crystal structure of the tyrosine kinase domain of the human insulin receptor Nature 372 1994 746 754
40. S.R. Hubbard Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog EMBO Journal 16 1997 5572 5581
41. M. Huse, and J. Kuriyan The conformational plasticity of protein kinases Cell 109 2002 275 282
42. S.C. Bresler, A.C. Wood, E.A. Haglund, J. Courtright, L.T. Belcastro, and J.S. Plegaria Differential inhibitor sensitivity of anaplastic lymphoma kinase variants found in neuroblastoma Science Translational Medicine 3 108 2011 108ra114
43. R.H. Palmer, E. Vernersson, C. Grabbe, and B. Hallberg Anaplastic lymphoma kinase: signalling in development and disease Biochemical Journal 420 2009 345 361
44. L. Wei, S.R. Hubbard, W.A. Hendrickson, and L. Ellis Expression, characterization, and crystallization of the catalytic core of the human insulin receptor protein-tyrosine kinase domain Journal of Biological Chemistry 270 1995 8122 8130
45. C.J. Tartari, R.H. Gunby, A.M. Coluccia, R. Sottocornola, B. Cimbro, and L. Scapozza Characterization of some molecular mechanisms governing autoactivation of the catalytic domain of the anaplastic lymphoma kinase Journal of Biological Chemistry 283 2008 3743 3750
46. R. Roskoski Jr. Structure and regulation of Kit protein-tyrosine kinase-the stem cell factor receptor Biochemical Biophysical Research Communications 338 2005 1307 1315
47. R. Chiarle, C. Voena, C. Ambrogio, R. Piva, and G. Inghirami The anaplastic lymphoma kinase in the pathogenesis of cancer Nature Reviews Cancer 8 2008 11 23
48. B. Vanhaesebroeck, L. Stephens, and P. Hawkins PI3K signalling: the path to discovery and understanding Nature Reviews Molecular Cell Biology 13 2012 195 203
49. R.R. Singh, J.H. Cho-Vega, Y. Davuluri, S. Ma, F. Kasbidi, and C. Milito Sonic hedgehog signaling pathway is activated in ALK-positive anaplastic large cell lymphoma Cancer Research 69 2009 2550 2558
50. M. Marzec, M. Kasprzycka, X. Liu, P.N. Raghunath, P. Wlodarski, and M.A. Wasik Oncogenic tyrosine kinase NPM/ALK induces activation of the MEK/ERK signaling pathway independently of c-Raf Oncogene 26 2007 813 821
51. J. Fujimoto, M. Shiota, T. Iwahara, N. Seki, H. Satoh, and S. Mori Characterization of the transforming activity of p80, a hyperphosphorylated protein in a Ki-1 lymphoma cell line with chromosomal translocation t(2;5) Proceedings of the National Academy of Sciences of the United States of America 93 1996 4181 4186
52. Q. Zhang, P.N. Raghunath, L. Xue, M. Majewski, D.F. Carpentieri, and N. Odum Multilevel dysregulation of STAT3 activation in anaplastic lymphoma kinase-positive T/null-cell lymphoma Journal of Immunology 168 2002 466 474
53. A.V. Galkin, J.S. Melnick, S. Kim, T.L. Hood, N. Li, and L. Li Identification of NVP-TAE684, a potent, selective, and efficacious inhibitor of NPM-ALK Proceedings of the National Academy of Sciences of the United States of America 104 2007 270 275 Erratum in: Proceedings of the National Academy of Sciences USA 2007;104:2025
54. H. Stein, D.Y. Mason, J. Gerdes, N. O'Connor, J. Wainscoat, and G. Pallesen The expression of the Hodgkin's disease associated antigen Ki-1 in reactive and neoplastic lymphoid tissue: evidence that Reed-Sternberg cells and histiocytic malignancies are derived from activated lymphoid cells Blood 66 1985 848 858
55. A.J. Ferreri, S. Govi, S.A. Pileri, and K.J. Savage Anaplastic large cell lymphoma, ALK-positive Critical Reviews in Oncology/Hematology 83 2012 293 302
56. J. Cools, I. Wlodarska, R. Somers, N. Mentens, F. Pedeutour, and B. Maes Identification of novel fusion partners of ALK, the anaplastic lymphoma kinase, in anaplastic large-cell lymphoma and inflammatory myofibroblastic tumor Genes, Chromosomes and Cancer 34 2002 354 362
57. L. Hernández, M. Pinyol, S. Hernández, S. Beà, K. Pulford, and A. Rosenwald TRK-fused gene (TFG) is a new partner of ALK in anaplastic large cell lymphoma producing two structurally different TFG-ALK translocations Blood 94 1999 3265 3268
58. L. Hernández, S. Beà, B. Bellosillo, M. Pinyol, B. Falini, and A. Carbone Diversity of genomic breakpoints in TFG-ALK translocations in anaplastic large cell lymphomas: identification of a new TFG-ALK(XL) chimeric gene with transforming activity American Journal of Pathology 160 2002 1487 1494
59. F. Tort, M. Pinyol, K. Pulford, G. Roncador, L. Hernandez, and I. Nayach Molecular characterization of a new ALK translocation involving moesin (MSN-ALK) in anaplastic large cell lymphoma Laboratory Investigation 81 2001 419 426
60. F. Tort, E. Campo, B. Pohlman, and E. Hsi Heterogeneity of genomic breakpoints in MSN-ALK translocations in anaplastic large cell lymphoma Human Pathology 35 2004 1038 1041
61. L. Lamant, N. Dastugue, K. Pulford, G. Delsol, and B. Mariamé A new fusion gene TPM3-ALK in anaplastic large cell lymphoma created by a (1;2)(q25;p23) translocation Blood 93 1999 3088 3095
62. R. Siebert, S. Gesk, L. Harder, D. Steinemann, W. Grote, and B. Schlegelberger Complex variant translocation t(1;2) with TPM3-ALK fusion due to cryptic ALK gene rearrangement in anaplastic large-cell lymphoma Blood 94 1999 3614 3617
63. S.J. Meech, L. McGavran, L.F. Odom, X. Liang, L. Meltesen, and J. Gump Unusual childhood extramedullary hematologic malignancy with natural killer cell properties that contains tropomyosin 4-anaplastic lymphoma kinase gene fusion Blood 98 2001 1209 1216
64. Z. Ma, J. Cools, P. Marynen, X. Cui, R. Siebert, and S. Gesk 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 95 2000 2144 2149
65. M. Trinei, L. Lanfrancone, E. Campo, K. Pulford, D.Y. Mason, and P.G. Pelicci A new variant anaplastic lymphoma kinase (ALK)-fusion protein (ATIC-ALK) in a case of ALK-positive anaplastic large cell lymphoma Cancer Research 60 2000 793 798
66. G.W. Colleoni, J.A. Bridge, B. Garicochea, J. Liu, D.A. Filippa, and M. Ladanyi 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 156 2000 781 789
67. L. Lamant, R.D. Gascoyne, M.M. Duplantier, F. Armstrong, A. Raghab, and M. Chhanabhai Non-muscle myosin heavy chain (MYH9): a new partner fused to ALK in anaplastic large cell lymphoma Genes, Chromosomes and Cancer 37 2003 427 432
68. C. Touriol, C. Greenland, L. Lamant, K. Pulford, F. Bernard, and T. Rousset 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 95 2000 3204 3207
69. K. Takeuchi, Y.L. Choi, Y. Togashi, M. Soda, S. Hatano, and K. Inamura KIF5B-ALK, a novel fusion oncokinase identified by an immunohistochemistry-based diagnostic system for ALK-positive lung cancer Clinical Cancer Research 15 2009 3143 3149
70. D.W. Wong, E.L. Leung, S.K. Wong, V.P. Tin, A.D. Sihoe, and L.C. Cheng A novel KIF5B-ALK variant in nonsmall cell lung cancer Cancer 117 2011 2709 2718
71. Y. Togashi, M. Soda, S. Sakata, E. Sugawara, S. Hatano, and R. Asaka KLC1-ALK: a novel fusion in lung cancer identified using a formalin-fixed paraffin-embedded tissue only PLoS One 7 2 2012 e31323
72. Y. Jung, P. Kim, Y. Jung, J. Keum, S.N. Kim, and Y.S. Choi Discovery of ALK-PTPN3 gene fusion from human non-small cell lung carcinoma cell line using next generation RNA sequencing Genes, Chromosomes and Cancer 51 2012 590 597
73. B. Lawrence, A. Perez-Atayde, M.K. Hibbard, B.P. Rubin, P. Dal Cin, and J.L. Pinkus TPM3-ALK and TPM4-ALK oncogenes in inflammatory myofibroblastic tumors American Journal of Pathology 157 2000 377 384
74. J.A. Bridge, M. Kanamori, Z. Ma, D. Pickering, D.A. Hill, and W. Lydiatt Fusion of the ALK gene to the clathrin heavy chain gene, CLTC, in inflammatory myofibroblastic tumor American Journal of Pathology 159 2001 411 415
75. A.S. Patel, K.M. Murphy, A.L. Hawkins, J.S. Cohen, P.P. Long, and E.J. Perlman RANBP2 and CLTC are involved in ALK rearrangements in inflammatory myofibroblastic tumors Cancer Genetics and Cytogenetics 176 2007 107 114
76. M. Debiec-Rychter, P. Marynen, A. Hagemeijer, and P. Pauwels ALK-ATIC fusion in urinary bladder inflammatory myofibroblastic tumor Genes, Chromosomes and Cancer 38 2003 187 190
77. L.V. Debelenko, D.C. Arthur, S.D. Pack, L.J. Helman, D.S. Schrump, and M. Tsokos Identification of CARS-ALK fusion in primary and metastatic lesions of an inflammatory myofibroblastic tumor Laboratory Investigation 83 2003 1255 1265
78. Z. Ma, D.A. Hill, M.H. Collins, S.W. Morris, J. Sumegi, and M. Zhou Fusion of ALK to the Ran-binding protein 2 (RANBP2) gene in inflammatory myofibroblastic tumor Genes, Chromosomes and Cancer 37 2003 98 105
79. A. Mariño-Enríquez, W.L. Wang, A. Roy, D. Lopez-Terrada, A.J. Lazar, and C.D. Fletcher Epithelioid inflammatory myofibroblastic sarcoma: an aggressive intra-abdominal variant of inflammatory myofibroblastic tumor with nuclear membrane or perinuclear ALK American Journal of Surgical Pathology 35 2011 135 144
80. I. Panagopoulos, T. Nilsson, H.A. Domanski, M. Isaksson, P. Lindblom, and F. Mertens Fusion of the SEC31L1 and ALK genes in an inflammatory myofibroblastic tumor International Journal of Cancer 118 2006 1181 1186
81. P. Adam, T. Katzenberger, H. Seeberger, S. Gattenlöhner, J. Wolf, and C. Steinlein A case of a diffuse large B-cell lymphoma of plasmablastic type associated with the t(2;5)(p23;q35) chromosome translocation American Journal of Surgical Pathology 27 2003 1473 1476
82. M. Onciu, F.G. Behm, J.R. Downing, S.A. Shurtleff, S.C. Raimondi, and Z. Ma ALK-positive plasmablastic B-cell lymphoma with expression of the NPM-ALK fusion transcript: report of 2 cases Blood 102 2003 2642 2644
83. P. De Paepe, M. Baens, H. van Krieken, B. Verhasselt, M. Stul, and A. Simons ALK activation by the CLTC-ALK fusion is a recurrent event in large B-cell lymphoma Blood 102 2003 2638 2641
84. K. Takeuchi, M. Soda, Y. Togashi, Y. Ota, Y. Sekiguchi, and S. Hatano Identification of a novel fusion, SQSTM1-ALK, in ALK-positive large B-cell lymphoma Haematologica 96 2011 464 467
85. C. Bedwell, D. Rowe, D. Moulton, G. Jones, N. Bown, and C.M. Bacon Cytogenetically complex SEC31A-ALK fusions are recurrent in ALK-positive large B-cell lymphomas Haematologica 96 2011 343 346
86. K. Van Roosbroeck, J. Cools, D. Dierickx, J. Thomas, P. Vandenberghe, and M. Stul ALK-positive large B-cell lymphomas with cryptic SEC31A-ALK and NPM1-ALK fusions Haematologica 95 2010 509 513
87. E. Lin, L. Li, Y. Guan, R. Soriano, C.S. Rivers, and S. Mohan Exon array profiling detects EML4-ALK fusion in breast, colorectal, and non-small cell lung cancers Molecular Cancer Research 7 2009 1466 1476
88. D. Lipson, M. Capelletti, R. Yelensky, G. Otto, A. Parker, and M. Jarosz Identification of new ALK and RET gene fusions from colorectal and lung cancer biopsies Nature Medicine 18 2012 382 384
89. F.R. Jazii, Z. Najafi, R. Malekzadeh, T.P. Conrads, A.A. Ziaee, and C. Abnet Identification of squamous cell carcinoma associated proteins by proteomics and loss of beta tropomyosin expression in esophageal cancer World Journal of Gastroenterology 12 2006 7104 7112
90. X.L. Du, H. Hu, D.C. Lin, S.H. Xia, X.M. Shen, and Y. Zhang Proteomic profiling of proteins dysregulated in Chinese esophageal squamous cell carcinoma Journal of Molecular Medicine 85 2007 863 875
91. L.V. Debelenko, S.C. Raimondi, N. Daw, B.R. Shivakumar, D. Huang, and M. Nelson Renal cell carcinoma with novel VCL-ALK fusion: new representative of ALK-associated tumor spectrum Modern Pathology 24 2011 430 442
92. L.G. Collins, C. Haines, R. Perkel, and R.E. Enck Lung cancer: diagnosis and management American Family Physician 75 2007 56 63
93. H.R. Sanders, H.R. Li, J.M. Bruey, J.A. Scheerle, A.M. Meloni-Ehrig, and J.C. Kelly Exon scanning by reverse transcriptase-polymerase chain reaction for detection of known and novel EML4-ALK fusion variants in non-small cell lung cancer Cancer Genetics 204 2011 45 52
94. Y. Li, X. Ye, J. Liu, J. Zha, and L. Pei Evaluation of EML4-ALK fusion proteins in non-small cell lung cancer using small molecule inhibitors Neoplasia 13 2011 1 11
95. A. Sandler, R. Gray, M.C. Perry, J. Brahmer, J.H. Schiller, and A. Dowlati Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer New England Journal of Medicine 355 2006 2542 2550
96. V.D. Cataldo, D.L. Gibbons, R. Pérez-Soler, and A. Quintás-Cardama Treatment of non-small-cell lung cancer with erlotinib or gefitinib New England Journal of Medicine 364 2011 947 955
97. G. Lenz, and L.M. Staudt Aggressive lymphomas New England Journal of Medicine 362 2010 1417 1429
98. B.D. Cheson, and J.P. Leonard Monoclonal antibody therapy for B-cell non-Hodgkin's lymphoma New England Journal of Medicine 359 2008 613 626
99. J.E. Butrynski, D.R. D'Adamo, J.L. Hornick, P. Dal Cin, C.R. Antonescu, and S.C. Jhanwar Crizotinib in ALK-rearranged inflammatory myofibroblastic tumor New England Journal of Medicine 363 2010 1727 1733
100. F. Armstrong, M.M. Duplantier, P. Trempat, C. Hieblot, L. Lamant, and E. Espinos Differential effects of X-ALK fusion proteins on proliferation, transformation, and invasion properties of NIH3T3 cells Oncogene 23 2004 6071 6082
101. J.M. Maris Recent advances in neuroblastoma New England Journal of Medicine 362 2010 2202 2211
102. A.K. Murugan, and M. Xing Anaplastic thyroid cancers harbor novel oncogenic mutations of the ALK gene Cancer Research 71 2011 4403 4411
103. H. Carén, F. Abel, P. Kogner, and T. Martinsson High incidence of DNA mutations and gene amplifications of the ALK gene in advanced sporadic neuroblastoma tumours Biochemical Journal 416 2008 153 159
104. F. Del Grosso, M. De Mariano, L. Passoni, R. Luksch, G.P. Tonini, and L. Longo Inhibition of N-linked glycosylation impairs ALK phosphorylation and disrupts pro-survival signaling in neuroblastoma cell lines BMC Cancer 11 2011 525
105. C. Lerch, and B. Richter Pharmacotherapy options for advanced thyroid cancer: a systematic review Drugs 72 2012 67 85
106. G. Nagaiah, A. Hossain, C.J. Mooney, J. Parmentier, and S.C. Remick Anaplastic thyroid cancer: a review of epidemiology, pathogenesis, and treatment Journal of Oncology 2011 2011 542358
107. R.L. Neff, W.B. Farrar, R.T. Kloos, and K.D. Burman Anaplastic thyroid cancer Endocrinology and Metabolism Clinics of North America 37 2008 52 58
108. Z. Burningham, M. Hashibe, L. Spector, and J.D. Schiffman The epidemiology of sarcoma Clinical Sarcoma Research 2 2012 14
109. R. Dasgupta, and D.A. Rodeberg Update on rhabdomyosarcoma Seminars in Pediatric Surgery 21 2012 68 78
110. J.C. van Gaal, U.E. Flucke, M.H. Roeffen, E.S. de Bont, S. Sleijfer, and A.M. Mavinkurve-Groothuis Anaplastic lymphoma kinase aberrations in rhabdomyosarcoma: clinical and prognostic implications Journal of Clinical Oncology 30 2012 308 315
111. L. Trusolino, A. Bertotti, and P.M. Comoglio MET signalling: principles and functions in development, organ regeneration and cancer Nature Reviews Molecular Cell Biology 11 2010 834 848
112. C.S. Cooper, M. Park, D.G. Blair, M.A. Tainsky, K. Huebner, and C.M. Croce Molecular cloning of a new transforming gene from a chemically transformed human cell line Nature 311 1984 29 33
113. J.J. Cui, M. Tran-Dubé, H. Shen, M. Nambu, P.P. Kung, and M. Pairish Structure based drug design of crizotinib (PF-02341066), a potent and selective dual inhibitor of mesenchymal-epithelial transition factor (c-MET) kinase and anaplastic lymphoma kinase (ALK) Journal of Medicinal Chemistry 54 2011 6342 6363
114. J.P. Eder, G.F. Vande Woude, S.A. Boerner, and P.M. LoRusso Novel therapeutic inhibitors of the c-Met signaling pathway in cancer Clinical Cancer Research 15 2009 2207 2214
115. S. Peters, and A.A. Adjei MET: a promising anticancer therapeutic target Nature Reviews Clinical Oncology 9 2012 314 326
116. E. Gherardi, W. Birchmeier, C. Birchmeier, and G. Vande Woude Targeting MET in cancer: rationale and progress Nature Reviews Cancer 12 2012 89 103
117. J. Gao, Y. Inagaki, P. Song, X. Qu, N. Kokudo, and W. Tang Targeting c-Met as a promising strategy for the treatment of hepatocellular carcinoma Pharmacological Research 65 2012 23 30
118. M.F. Di Renzo, M. Olivero, T. Martone, A. Maffe, P. Maggiora, and A.D. Stefani Somatic mutations of the MET oncogene are selected during metastatic spread of human HNSC carcinomas Oncogene 19 2000 1547 1555
119. X. Xin, S. Yang, G. Ingle, C. Zlot, L. Rangell, and J. Kowalski Hepatocyte growth factor enhances vascular endothelial growth factor-induced angiogenesis in vitro and in vivo American Journal of Pathology 158 2001 1111 1120
120. R. Roskoski Jr. Vascular endothelial growth factor (VEGF) signaling in tumor progression Critical Reviews in Oncology/Hematology 62 2007 179 213
121. J.G. Christensen, H.Y. Zou, M.E. Arango, Q. Li, J.H. Lee, and S.R. McDonnell Cytoreductive antitumor activity of PF-2341066, a novel inhibitor of anaplastic lymphoma kinase and c-Met, in experimental models of anaplastic large-cell lymphoma Molecular Cancer Therapy 6 2007 3314 3322
122. E.L. Kwak, Y.J. Bang, D.R. Camidge, A.T. Shaw, B. Solomon, and R.G. Maki Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer New England Journal of Medicine 363 2010 1693 1703 Erratum in: New England Journal of Medicine 2011;364:588
123. D.R. Camidge, and R.C. Doebele Treating ALK-positive lung cancer-early successes and future challenges Nature Reviews Clinical Oncology 9 2012 268 277
124. E. Winer, J. Gralow, L. Diller, B. Karlan, P. Loehrer, and L. Pierce Clinical cancer advances 2008: major research advances in cancer treatment, prevention, and screening-a report from the American Society of Clinical Oncology Journal of Clinical Oncology 27 2009 812 826 Erratum in: Journal of Clinical Oncology 2009;27:3070-1
125. R. Katayama, A.T. Shaw, T.M. Khan, M. Mino-Kenudson, B.J. Solomon, and B. Halmos Mechanisms of acquired crizotinib resistance in ALK-rearranged lung Cancers Science Translational Medicine 4 2012 120ra17
126. T. Sasaki, K. Okuda, W. Zheng, J. Butrynski, M. Capelletti, and L. Wang The neuroblastoma-associated F1174L ALK mutation causes resistance to an ALK kinase inhibitor in ALK-translocated cancers Cancer Research 70 2010 10038 10043
127. Y.L. Choi, M. Soda, Y. Yamashita, T. Ueno, J. Takashima, and T. Nakajima EML4-ALK mutations in lung cancer that confer resistance to ALK inhibitors New England Journal of Medicine 363 2010 1734 1739
128. F. Zuccotto, E. Ardini, E. Casale, and M. Angiolini Through the gatekeeper door: exploiting the active kinase conformation Journal of Medicinal Chemistry 53 2010 2681 2694
129. M. Azam, M.A. Seeliger, N.S. Gray, J. Kuriyan, and G.Q. Daley Activation of tyrosine kinases by mutation of the gatekeeper threonine Nature Structural & Molecular Biology 15 2008 1109 1118
130. C.M. Lovly, J.M. Heuckmann, E. de Stanchina, H. Chen, R.K. Thomas, and C. Liang Insights into ALK-driven cancers revealed through development of novel ALK tyrosine kinase inhibitors Cancer Research 71 2011 4920 4931
131. C.M. Lovly, and W. Pao Escaping ALK inhibition: mechanisms of and strategies to overcome resistance Science Translational Medicine 4 120 2012 120ps2
132. T. Sasaki, J. Koivunen, A. Ogino, M. Yanagita, S. Nikiforow, and W. Zheng A novel ALK secondary mutation and EGFR signaling cause resistance to ALK kinase inhibitors Cancer Research 71 2011 6051 6060
133. R.C. Doebele, A.B. Pilling, D.L. Aisner, T.G. Kutateladze, A.T. Le, and A.J. Weickhardt Mechanisms of resistance to crizotinib in patients with ALK gene rearranged non-small cell lung cancer Clinical Cancer Research 18 2012 1472 1482
134. J.M. Heuckmann, M. Hölzel, M.L. Sos, S. Heynck, H. Balke-Want, and M. Koker ALK mutations conferring differential resistance to structurally diverse ALK inhibitors Clinical Cancer Research 17 2011 7394 7401
135. R. Katayama, T.M. Khan, C. Benes, E. Lifshits, H. Ebi, and V.M. Rivera Therapeutic strategies to overcome crizotinib resistance in non-small cell lung cancers harboring the fusion oncogene EML4-ALK Proceedings of the National Academy of Sciences of the United States of America 108 2011 7535 7540
136. R. Roskoski Jr. STI-571: an anticancer protein-tyrosine kinase inhibitor Biochemical Biophysical Research Communications 309 2003 709 717
137. K. Kinoshita, K. Asoh, N. Furuichi, T. Ito, H. Kawada, and S. Hara Design and synthesis of a highly selective, orally active and potent anaplastic lymphoma kinase inhibitor (CH5424802) Bioorganic and Medicinal Chemistry 20 2012 1271 1280
138. H. Sakamoto, T. Tsukaguchi, S. Hiroshima, T. Kodama, T. Kobayashi, and T.A. Fukami CH5424802, a selective ALK inhibitor capable of blocking the resistant gatekeeper mutant Cancer Cell 19 2011 679 690
139. K. Kinoshita, T. Kobayashi, K. Asoh, N. Furuichi, T. Ito, and H. Kawada 9-Substituted 6,6-dimethyl-11-oxo-6,11-dihydro-5H-benzo[b]carbazoles as highly selective and potent anaplastic lymphoma kinase inhibitors Journal of Medicinal Chemistry 54 2011 6286 6294
140. S. Kuromitsu, M. Mori, I. Shimada, Y. Kondoh, N. Shindoh, and T. Soga Antitumor activities of ASP3026 against EML4-ALK-dependent tumor models Molecular Cancer Therapeutics 10 11 Suppl. 2011 Abstract A227
141. P. Sabbatini, S. Korenchuk, J.L. Rowand, A. Groy, Q. Liu, and D. Leperi GSK1838705A inhibits the insulin-like growth factor-1 receptor and anaplastic lymphoma kinase and shows antitumor activity in experimental models of human cancers Molecular Cancer Therapeutics 8 2009 2811 2820
142. M. Cheng, M.R. Quail, D.E. Gingrich, G.R. Ott, L. Lu, and W. Wan CEP-28122, a highly potent and selective orally active inhibitor of anaplastic lymphoma kinase with antitumor activity in experimental models of human cancers Molecular Cancer Therapy 11 2012 67 69
143. D.E. Gingrich, J.G. Lisko, M.A. Curry, M. Cheng, M. Quail, and L. Lu Discovery of an orally efficacious inhibitor of anaplastic lymphoma kinase Journal of Medicinal Chemistry 55 2012 4580 4593
144. G.R. Ott, G.J. Wells, T.V. Thieu, M.R. Quail, J.G. Lisko, and E.F. Mesaros 2,7-Disubstituted-pyrrolo[2,1-f][1,2,4]triazines: new variant of an old template and application to the discovery of anaplastic lymphoma kinase (ALK) inhibitors with in vivo antitumor activity Journal of Medicinal Chemistry 54 2011 6328 6341
145. R.T. Lewis, C.M. Bode, D.M. Choquette, M. Potashman, K. Romero, and J.C. Stellwagen The discovery and optimization of a novel class of potent, selective, and orally bioavailable anaplastic lymphoma kinase (ALK) inhibitors with potential utility for the treatment of cancer Journal of Medicinal Chemistry 55 2012 6523 6540
146. C.A. Lipinski, F. Lombardo, B.W. Dominy, and P.J. Feeney Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings Advanced Drug Delivery Reviews 23 1997 3 25
147. G.F. Smith Medicinal chemistry by the numbers: the physicochemistry, thermodynamics and kinetics of modern drug design Progress in Medicinal Chemistry 48 2009 1 29
148. P.D. Leeson, and B. Springthorpe The influence of drug-like concepts on decision-making in medicinal chemistry Nature Reviews Drug Discovery 6 2007 881 890
149. J.D. Rowley Letter: a new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining Nature 243 1973 290 293
150. J. Groffen, J.R. Stephenson, N. Heisterkamp, A. de Klein, C.R. Bartram, and G. Grosveld Philadelphia chromosomal breakpoints are clustered within a limited region, bcr, on chromosome 22 Cell 36 1984 93 99
151. J.S. Khorashad, and M.W. Deininger Selection of therapy: rational decisions based on molecular events Hematology/Oncology Clinics of North America 25 2011 1009 1023
152. T.P. Hughes, A. Hochhaus, S. Branford, M.C. Müller, J.S. Kaeda, and L. Foroni Long-term prognostic significance of early molecular response to imatinib in newly diagnosed chronic myeloid leukemia: an analysis from the International Randomized Study of Interferon and STI571 (IRIS) Blood 116 2010 3758 3765
153. H. Kantarjian, C. Sawyers, A. Hochhaus, F. Guilhot, C. Schiffer, and C. Gambacorti-Passerini Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia New England Journal of Medicine 346 2002 645 652 Erratum in: New England Journal of Medicine 2002;346:1923
154. E. Jabbour, S.A. Parikh, H. Kantarjian, and J. Cortes Chronic myeloid leukemia: mechanisms of resistance and treatment Hematology/Oncology Clinics of North America 25 2011 981 995
155. M. Ohanian, J. Cortes, H. Kantarjian, and E. Jabbour Tyrosine kinase inhibitors in acute and chronic leukemias Expert Opinion on Pharmacotherapy 13 2012 927 938
156. R. Roskoski Jr. The ErbB/HER receptor protein-tyrosine kinases and cancer Biochemical and Biophysical Research Communications 319 2004 1 11
157. G. Ghosh, X. Lian, S.J. Kron, and S.P. Palecek Properties of resistant cells generated from lung cancer cell lines treated with EGFR inhibitors BMC Cancer 12 2012 95
158. W. Pao, V.A. Miller, K.A. Politi, G.J. Riely, R. Somwar, and M.F. Zakowski Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain PLoS Medicine 2 3 2005 e73
159. C.H. Yun, K.E. Mengwasser, A.V. Toms, M.S. Woo, H. Greulich, and K.K. Wong The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP Proceedings of the National Academy of Sciences of the United States of America 105 2008 2070 2075
160. K.T. Flaherty, I. Puzanov, K.B. Kim, A. Ribas, G.A. McArthur, and J.A. Sosman Inhibition of mutated, activated BRAF in metastatic melanoma New England Journal of Medicine 363 2010 809 819
161. R.S. Tuma Getting around PLX4032: studies turn up unusual mechanisms of resistance to melanoma drug Journal of the National Cancer Institute 103 2011 170 177
162. H.Y. Zou, Q. Li, J.H. Lee, M.E. Arango, S.R. McDonnell, and S. Yamazaki An orally available small-molecule inhibitor of c-Met, PF-2341066, exhibits cytoreductive antitumor efficacy through antiproliferative and antiangiogenic mechanisms Cancer Research 67 2007 4408 4417
163. D.E. Gerber, and J.D. Minna ALK inhibition for non-small cell lung cancer: from discovery to therapy in record time Cancer Cell 18 2010 548 551
164. B.J. Druker, and N.B. Lydon Lessons learned from the development of an abl tyrosine kinase inhibitor for chronic myelogenous leukemia Journal of Clinical Investigation 105 2000 3 7
165. R. Roskoski Jr. RAF protein-serine/threonine kinases: structure and regulation Biochemical Biophysical Research Communications 399 2010 313 317