ALK inhibitors and advanced non-small cell lung cancer (Review)

International Journal of Oncology

Volumn 45, Issue 2, 2014, Pages 499-508

  Rossi, Antonio ^a   Maione, Paolo ^a   Sacco, Paola Claudia ^a   Sgambato, Assunta ^b   Casaluce, Francesca ^b   Ferrara, Marianna Luciana ^b   Palazzolo, Giovanni ^c   Ciardiello, Fortunato ^b   Gridelli, Cesare ^a  

^a S G MOSCATI HOSPITAL   (Italy)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

^c Division of Radiation Oncology   (Italy)

Author keywords

ALK; Brain metastases; Crizotinib; HSP90 inhibitors; LDK378; Mechanisms of resistance; NSCLC; Pemetrexed; ROS1

Indexed keywords

AFATINIB; ALANINE AMINOTRANSFERASE; ALECTINIB; AP 26113; BEVACIZUMAB; CARBOPLATIN; CERITINIB; CRIZOTINIB; DOCETAXEL; DSB AP 26113; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GANETESPIB; GEFITINIB; HEAT SHOCK PROTEIN 90 INHIBITOR; K RAS PROTEIN; LUMINESPIB; PACLITAXEL; PEMETREXED; PROTEIN TYROSINE KINASE INHIBITOR; SCATTER FACTOR RECEPTOR; THYMIDYLATE SYNTHASE; UNCLASSIFIED DRUG; ANAPLASTIC LYMPHOMA KINASE; ANTINEOPLASTIC AGENT; PROTEIN KINASE INHIBITOR; PROTEIN TYROSINE KINASE;

ADVANCED CANCER; BRAIN METASTASIS; CANCER SURVIVAL; DIARRHEA; DRUG EFFICACY; DRUG WITHDRAWAL; HUMAN; HYPOPHOSPHATEMIA; LUNG NON SMALL CELL CANCER; LYMPHOCYTOPENIA; MUTATION; NEUTROPENIA; OVERALL SURVIVAL; POINT MUTATION; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; REVIEW; SIDE EFFECT; ANTAGONISTS AND INHIBITORS; CARCINOMA, NON-SMALL-CELL LUNG; ENZYMOLOGY; GENETICS; LUNG NEOPLASMS;

ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; HUMANS; LUNG NEOPLASMS; PROTEIN KINASE INHIBITORS; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 84902584129     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2014.2475     Document Type: Review

References (80)

1. Rossi A, Torri V, Garassino MC, Porcu L and Galetta D: The impact of personalized medicine on survival: comparisons of results in metastatic breast, colorectal and non-small-cell lung cancers. Cancer Treat Rev 40: 485-494 2014.
2. Scagliotti GV, Parikh P, von Pawel J, et al: Phase III study comparing cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapy-naive patients with advanced-stage non-small-cell lung cancer. J Clin Oncol 26: 3543-3551, 2008.
3. Sandler A, Gray R, Perry MC, et al: Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med 355: 2542-2550, 2006. (Pubitemid 44917502)
4. Rossi A, Pasquale R, Esposito C and Normanno N: Should epidermal growth factor receptor tyrosine kinae inhibitors be considered ideal drugs for the treatment of selected advanced non-small cell lung cancer patients? Cancer Treat Rev 39: 489-497, 2013.
5. Soda M, Choi YL, Enomoto M, et al: Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 448: 561-566, 2007. (Pubitemid 47206930)
6. + anaplastic large-cell lymphoma. Blood 110: 2259-2267, 2007.
7. Chiarle R, Voena C, Ambrogio C, Piva R and Inghirami G: The anaplastic lymphoma kinase in the pathogenesis of cancer. Nat Rev Cancer 8: 11-23, 2008.
8. Sasaki T, Rodig SJ, Cirieac LR and Janne PA: The biology and treatment of EML4-ALK non-small cell lung cancer. Eur J Cancer 46: 1773-1780, 2010.
9. Takeuchi K, Choi YL, Togashi Y, et al: KIF5B-ALK, a novel fusion oncokinase identified by an immunohistochemistry-based diagnostic system for ALK-positive lung cancer. Clin Cancer Res 15: 3143-3149, 2009.
10. Rikova K, Guo A, Zeng Q, et al: Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 131: 1190-1203, 2007. (Pubitemid 350235027)
11. Inamura K, Takeuchi K, Togashi Y, et al: EML4-ALK fusion is linked to histological characteristics in a subset of lung cancers. J Thorac Oncol 3: 13-17, 2008.
12. Rodig SJ, Mino-Kenudson M, Dacic S, et al: Unique clinicopathologic features characterize ALK-rearranged lung adenocarcinoma in the western population. Clin Cancer Res 15: 5216-5223, 2009.
13. Shaw AT, Yeap BY, Mino-Kenudson M, et al: Clinical features and outcome of patients with non-small-cell lung cancer who harbor EML4-ALK. J Clin Oncol 27: 4247-4253, 2009.
14. Wong DW, Leung EL, So KK, et al: The EML4-ALK fusion gene is involved in various histologic types of lung cancers from nonsmokers with wild-type EGFR and KRAS. Cancer 115: 1723-1733, 2009.
15. Zhang X, Zhang S, Yang X, et al: Fusion of EML4 and ALK is associated with development of lung adenocarcinomas lacking EGFR and KRAS mutations and is correlated with ALK expression. Mol Cancer 9: 188, 2010.
16. Koh Y, Kim DW, Kim TM, et al: Clinicopathologic characteristics and outcomes of patients with anaplastic lymphoma kinase-positive advanced pulmonary adenocarcinoma. J Thorac Oncol 6: 905-912, 2011.
17. Barlesi F, Blons H, Beau-Faller M, et al: Biomarkers (BM) France: results of routine EGFR, HER2, KRAS, BRAF, PI3KCA mutations detection and EML4-ALK gene fusion assessment on the first 10,000 non-small cell lung cancer (NSCLC) patients (pts). J Clin Oncol 31: 8000, 2013.
18. Johnson BE, Kris MG, Berry LD, et al: A multicenter effort to identify driver mutations and employ targeted therapy in patients with lung adenocarcinomas: The Lung Cancer Mutation Consortium (LCMC). J Clin Oncol 31: 8019, 2013.
19. Rosell R, Massuti Sureda B, Costa C, et al : Concomitant actionable mutations and overall survival (OS) in EGFR-mutant non-small-cell lung cancer (NSCLC) patients (p) included in the EURTAC trial: EGFR L858R, EGFR T790M, TP53 R273H and EML4-ALK. Ann Oncol 23 (Suppl 9): ixe22 (LBA31), 2012.
20. Rosell R, Carcereny E, Gervais R, et al: Erlotinib versus standard chemotherapy as first-line treatment for European patients with advanced EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicenter, open-label, randomised phase 3 trial. Lancet Oncol 13: 239-246, 2012.
21. Lindeman NI, Cagle PT, Beasley MB, et al: Molecular testing guidelinefor selection of lung cancer patients for EGFR and ALK tyrosine kinase inhibitors; guideline from the College of American Pathologists, International Association for the Study of Lung Cancer, and Association for Molecular Pathology. J Thorac Oncol 8: 823-859, 2013.
22. Camidge DR, Kono SA, Flacco A, 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 16: 5581-5590, 2010.
23. Park HS, Lee JK, Kim DW, et al: Immunohistochemical screening for anaplastic lymphoma kinase (ALK) rearrangement in advanced non-small cell lung cancer patients. Lung Cancer 77: 288-292, 2012.
24. Minca EC, Portier BP, Wang Z, et al: ALK status testing in non-small cell lung carcinoma: correlation between ultrasensitive IHC and FISH. J Mol Diagn 15: 341-346, 2013.
25. Sholl LM, Weremowicz S, Gray SW, et al: Combined use of ALK immunohistochemistry and FISH for optimal detection of ALK-rearranged lung adenocarcinomas. J Thorac Oncol 8: 322-328, 2013.
26. Martinez P, Hernández-Losa J, Montero MÁ, et al.: Fluorescence in situ hybridization and immunohistochemistry as diagnostic methods for ALK positive non-small cell lung cancer patients. PLoS One 8: e52261, 2013.
27. Conklin CM, Craddock KJ, Have C, et al: Immunohistochemistry is a reliable screening tool for identification of ALK rearrangement in non-small-cell lung carcinoma and is antibody dependent. J Thorac Oncol 8: 45-51, 2013.
28. Christensen JG, Zou HY, Arango ME, et al: Cytoreductive antitumor activity of PF-2341066, a novel inhibitor of anaplastic lymphoma kinase and c-Met, in experimental models of anaplastic large-cell lymphoma. Mol Cancer Ther 6: 3314-3322, 2007.
29. Cui JJ, Tran-Dubé M, Shen H, et al.: 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). J Med Chem 54: 6342-6363, 2011.
30. Kwak EL, Camidge DR, Clark J, et al.: Clinical activity observed in a phase I dose escalation trial of an oral c-met and ALK inhibitor, PF-02341066. J Clin Oncol 27 (15S): 148s, 3509, 2009.
31. Kwak EL, Bang YJ, Camidge DR, et al: Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med 363: 1693-1703, 2010.
32. Camidge DR, Bang Y-B, Kwak EL, et al: Activity and safety of crizotinib in patients with ALK-positive non-small-cell lung cancer: updated results from a phase 1 study. Lancet Oncol 13: 1011-1019, 2012.
33. Shaw AT, Yeap BY, Solomon BJ, et al: Effect of crizotinib on overall survival in patients with advanced non-small-cell lung cancer harbouring ALK gene rearrangement: a retrospective analysis. Lancet Oncol 12: 1004-1012, 2011.
34. Kim D, Ahn M, Yang P, et al.: Updated results of a global phase II study with crizotinib in advanced ALK-positive non-small cell lung cancer (NSCLC). Ann Oncol 23 (Suppl 9): ix402, 1230PD, 2012.
35. Shaw AT, Kim DW, Nakagawa K, et al.: Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N Engl J Med 368: 2385-2394, 2013.
36. Weickhardt AJ, Rothman MS, Salian-Mehta S, et al.: Rapid-onset hypogonadism secondary to crizotinib use in men with metastatic nonsmall cell lung cancer. Cancer 118: 5302-5309, 2012.
37. Weickhardt AJ, Doebele RC, Purcell WT, et al: Symptomatic reduction in free testosterone levels secondary to crizotinib use in male cancer patients. Cancer 119: 2383-2390, 2013.
38. A clinical trial testing the efficacy of crizotinib versus standard chemotherapy pemetrexed plus cisplatin or carboplatin in patients with ALK positive non squamous cancer of the lung (PROFILE 1014). http://clinicaltrials. gov/ct2/show/NCT01154140. Accessed March 15, 2014.
39. Choi YL, Soda M, Yamashita Y, et al.: EML4-ALK mutations in lung cancer that confer resistance to ALK inhibitors. N Engl J Med 363: 1734-1739, 2010.
40. Sasaki T, Koivunen J, Ogino A, et al: A novel ALK secondary mutation and EGFR signaling cause resistance to ALK kinase inhibitors. Cancer Res 71: 6051-6060, 2011.
41. Katayama R, Khan TM, Benes C, et al: Therapeutic strategies to overcome crizotinib resistance in non-small cell lung cancers harboring the fusion oncogene EML4-ALK. Proc Natl Acad Sci USA 108: 7535-7540, 2011.
42. Zhang S, Wang F, Keats J, et al: Crizotinib-resistant mutants of EML4-ALK identified through an accelerated mutagenesis screen. Chem Biol Drug Des 78: 999-1005, 2011.
43. Katayama R, Shaw AT, Khan TM, et al.: Mechanisms of acquired crizotinib resistance in ALK-rearranged lung cancers. Sci Transl Med 4: 120ra17, 2012.
44. Doebele RC, Pilling AB, Aisner DL, et al: Mechanisms of resistance to crizotinib in patients with ALK gene rearranged non-small cell lung cancer. Clin Cancer Res 18: 1472-1482, 2012.
45. Lovly CM and Pao W: Escaping ALK inhibition: mechanisms of and strategies to overcome resistance. Sci Transl Med 4: 120ps2, 2012.
46. Doebele RC, Aisner DL, Le AT, et al: Analysis of resistance mechanisms to ALK kinase inhibitors in ALK+ NSCLC patients. J Clin Oncol 30 (15S): 7504, 2012.
47. Camidge DR, Bang Y, Kwak EL, et al.: Progression-free survival (PFS) from a phase I study of crizotinib (PF-02341066) in patients with ALK-positive non-small cell lung cancer (NSCLC). J Clin Oncol 29 (15S): 2501, 2011.
48. Shaw AT, Mehra R, Kim DW, et al.: Clinical activity of the ALK inhibitor LDK378 in advanced, ALK-positive NSCLC. J Clin Oncol 31 (15S): 8010, 2013.
49. Shaw AT, Mok T, Spigel DR, et al.: A phase II single-arm study of LDK378 in patients with ALK-activated (ALK+) non-small cell lung cancer (NSCLC) previously treated with chemotherapy and crizotinib (CRZ). J Clin Oncol 31 (15S): TPS8119, 2013.
50. Seto T, Kiura K, Nishio M, et al: CH5424802 (RO5424802) for patients with ALK-rearranged advanced non-small-cell lung cancer (AF-001JP study): a single-arm, open-label, phase 1-2 study. Lancet Oncol 14: 590-598, 2013.
51. Gadgeel S, Ou SH, Chiappori AA, et al: A Phase 1 dose escalation study of a new ALK inhibitor, CH5424802/RO5424802, in ALK+ non-small cell lung cancer (NSCLC) patients who have failed crizotinib (AF-002JG/NP28761, NCT01588028). J Thorac Oncol 8 (Suppl 2): S199, O16.06, 2013.
52. A study of RO5424802 in patients with non-small cell lung cancer who have ALK mutation and failed crizotinib treatment. http://clinicaltrials.gov/show/ NCT01801111. Accessed March 15, 2014.
53. Camidge DR, Bazhenova L, Salgia R, et al.: First-in-human dose-finding study of the ALK/EGFR inhibitor AP26113 in patients with advanced malignancies: updated results. J Clin Oncol 31 (15S): 8031, 2013.
54. Chen Z, Sasaki T, Tan X, et al.: Inhibition of ALK, PI3K/MEK, and HSP90 in murine lung adenocarcinoma induced by EML4-ALK fusion oncogene. Cancer Res 70: 9827-9836, 2010.
55. Socinski MA, Goldman J, El-Hariry I, et al: A multicenter phase II study of ganetespib monotherapy in patients with genotypically defined advanced non-small cell lung cancer. Clin Cancer Res 19: 3068-3077, 2013.
56. Sequist LV, Gettinger S, Senzer NN, et al: Activity of IPI-504, a novel heat-shock protein 90 inhibitor, in patients with molecularly defined non-small-cell lung cancer. J Clin Oncol 28: 4953-4960, 2010.
57. +) or EGFR-mutated advanced non-small cell lung cancer (NSCLC). Ann Oncol 23 (Suppl 9): ix152-ix174, 438, 2012.
58. A study of ganetespib in subjects with ALK-positive non-small-cell lung cancer (NSCLC) (CHIARA). http://clinicaltrials.gov/show/NCT01562015. Accessed March 15, 2014.
59. Crizotinib and ganetespib (STA-9090) in ALK positive lung cancers. http://clinicaltrials.gov/show/NCT01579994. Accessed March 15, 2014.
60. AUY922 for advanced ALK-positive NSCLC. http://clinical-trials.gov/show/ NCT01752400. Accessed March 15, 2014.
61. Phase Ib study of LDK378 and AUY922 in ALK-rearranged non-small cell lung cancer. http://clinicaltrials.gov/show/NCT01772797. Accessed March 15, 2014.
62. Camidge DR, Kono SA, Lu X, et al: Anaplastic lymphoma kinase gene rearrangements in non-small cell lung cancer are associated with prolonged progression-free survival on pemetrexed. J Thorac Oncol 6: 774-780, 2011.
63. Lee JO, Kim TM, Lee SH, et al: Anaplastic lymphoma kinase translocation: a predictive biomarker of pemetrexed in patients with non-small cell lung cancer. J Thorac Oncol 6: 1474-1480, 2011.
64. Takezawa K, Okamoto I, Okamoto W, et al : Thymidylate synthase as a determinant of pemetrexed sensitivity in non-small cell lung cancer. Br J Cancer 104: 1594-1601, 2011.
65. Shaw AT, Varghese AM, Solomon BJ, et al: Pemetrexed-based chemotherapy in patients with advanced, ALK-positive non-small cell lung cancer. Ann Oncol 24: 59-66, 2013.
66. Rimkunas VM, Crosby KE, Li D, 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 18: 4449-4457, 2012.
67. Takeuchi K, Soda M, Togashi Y, et al: RET, ROS1 and ALK fusions in lung cancer. Nat Med 18: 378-381, 2012.
68. Bergethon K, Shaw AT, Ou SH, et al: ROS1 rearrangements define a unique molecular class of lung cancers. J Clin Oncol 30: 863-870, 2012.
69. Yasuda H, de Fiqueiredo-Pontes LL, Kobayashi S and Costa DB: Preclinical rationale for use of the clinically available multi-targeted tyrosine kinase inhibitor crizotinib in ROS1-translocated lung cancer. J Thorac Oncol 7: 1086-1090, 2012.
70. Shaw AT, Camidge DR, Engelman JA, et al: Clinical activity of crizotinib in advanced non-small cell lung cancer (NSCLC) harboring ROS1 gene rearrangement. J Clin Oncol 30 (15S): 7508, 2012.
71. Awad MM, Katayama R, McTigue M, et al.: Acquired resistance to crizotinib from a mutation in CD74-ROS1. N Engl J Med 368; 2395-2401, 2013.
72. Weickhardt AJ, Scheier B, Burke JM, et al: Local ablative therapy of oligoprogressive disease prolongs disease control by tyrosine kinase inhibitors in oncogene addicted non-small cell lung cancer. J Thorac Oncol 7: 1807-1814, 2012.
73. Costa DB, Kobayashi S, Pandya SS and Yeo WL: CSF concentration of the anaplastic lymphoma kinase inhibitor crizotinib. J Clin Oncol 29: e443-e445, 2012.
74. Chun SG, Choe KS, Iyengar P, Yordy JS and Timmerman RD: Isolated central nervous system progression on crizotinib: an Achilles heel of non-small cell lung cancer with EML4-ALK translocations? Cancer Biol Ther 13: 1376-1383, 2012.
75. Maillet D, Martel-Lafay I, Arpin D and Perol M: Ineffectiveness of crizotinib on brain metastases in two cases of lung adenocarcinoma with EML4-ALK rearrangement. J Thorac Oncol 8: e30-e31, 2013.
76. Kim YH, Ozasa H, Nagai H, et al: High-dose crizotinib for brain metastases refractory to standard-dose crizotinib. J Thorac Oncol 8: e85-e86, 2013.
77. Kinoshita Y, Koga Y, Sakamoto A and Hidaka K: Long-lasting response to crizotinib in brain metastases due to EML4-ALK-rearranged non-small-cell lung cancer. BMJ Case Rep 2013 doi: 10.1136/bcr-2013-200867.
78. Peled N, Zach L, Liran O, Ilouze M, Bunn PA Jr and Hirsch FR: Effective crizotinib schedule for brain metastases in ALK rearrangement metastatic non-small-cell lung cancer. J Thorac Oncol 8: e112-e113, 2013.
79. Ou SH, Gadgeel S, Chiappori AA, et al: Consistent therapeutic efficacy of CH5424802/RO5424802 in brain metastases among crizotinib-refractory ALK-positive non-small cell lung cancer (NSCLC) patients in an ongoing phase I/II study (AF-002JG/NP28761, NCT01588028). J Thorac Oncol 8 (Suppl 2): S200 O16.07, 2013.
80. Loscher W and Potschka H: Blood-brain barrier active efflux transporters: ATP-binding cassette gene family. NeuroRx 2: 86-98, 2005. (Pubitemid 40128029)