Will the requirement by the US FDA to simultaneously co-develop companion diagnostics (CDx) delay the approval of receptor tyrosine kinase inhibitors for RTK-rearranged (ROS1-, RET-, AXL-, PDGFR-α-, NTRK1-) non-small cell lung cancer globally?

Frontiers in Oncology

Volumn 4 APR, Issue , 2014, Pages

  Ou, Sai Hong Ignatius ^a   Soo, Ross A ^b   Kubo, Akihito ^c   Kawaguchi, Tomoya ^d   Ahn, Myung Ju ^e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

^c AICHI MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d NATIONAL HOSPITAL ORGANIZATION KINKI CHUO CHEST MEDICAL CENTER   (Japan)

^e Sungkyunkwan University School of Medicine   (South Korea)

Author keywords

ALK rearranged NSCLC; Companion diagnostics; Fluorescence in situ hybridization; Immunohistochemistry; Next generation sequencing; RET rearranged NSCLC; Reverse transcription polymerase chain reaction; ROS1 rearranged NSCLC

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CABOZANTINIB; CD74 ANTIGEN; CRIZOTINIB; LENVATINIB; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PONATINIB; PROTEIN RET; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE A; PROTEIN TYROSINE KINASE INHIBITOR; RAF PROTEIN; REGORAFENIB; SORAFENIB; SUNITINIB; VANDETANIB; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 3;

BREAST CANCER; CHRONIC MYELOMONOCYTIC LEUKEMIA; CLINICAL TRIAL (TOPIC); COLORECTAL CARCINOMA; COST EFFECTIVENESS ANALYSIS; DNA TRANSFECTION; DRUG APPROVAL; DRUG INDUSTRY; FLUORESCENCE IN SITU HYBRIDIZATION; FOOD AND DRUG ADMINISTRATION; GENE REARRANGEMENT; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG NON SMALL CELL CANCER; MOLECULAR DIAGNOSTICS; OFF LABEL DRUG USE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; THYROID CANCER;

EID: 84901002216     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00058     Document Type: Review

References (42)

1. Ou SI, Barlett CH, Mino-Kneudson M, Cui J, Iafrate AJ. Crizotinib for the treatment of ALK-rearranged non-small cell lung cancer: a success story to usher in the second decade of molecular targeted therapy in oncology. Oncologist (2012) 17:1351-75. doi: 10.1634/theoncologist.2012-0311.
2. Gainor JF, Shaw AT. Novel targets in non-small cell lung cancer. ROS1 and RET fusions. Oncologist (2013) 18:865-75. doi:10.1634/theoncologist.2013-0095.
3. Seo J, Ju YS, Lee W, Shin J, Lee JK, Bleazard T, et al. The transcriptional landscape and mutational profile of lung adenocarcinoma. Genome Res (2012) 22:2109-19. doi:10.1101/gr.145144.112.
4. Vaishnavi A, Capelletti M, Le AT, Kako S, Butaney M, Ercan D, et al. Oncogenic and drug-sensitive NTRK1 rearrangement in lung cancer. Nat Med (2013) 19:1469-72. doi:10.1038/nm.3352.
5. Wilheim SM, Dumas J, Adnane L, Lynch M, Carter CA, Schutz G, et al. Regoragenib (BAY 73-4506): a new oral multikinase inhibitor of angiogenic, stromal and oncogenic receptor tyrosine kinases with potent preclinical antitumor activity. Int J Cancer (2011) 129:245-55. doi:10.1002/ijc.25864.
6. Mologni L, Radaelli S, Morandi A, Plaza-Menacho I, Gambacorti-Passerini C. Ponatinib is a potent inhibitor of wild-type and drug-resistant gatekeeper mutant RET kinase. Mol Cell Endocrinol (2013) 377:1-6. doi:10.1016/j.mce.2013.06.025.
7. Bentzien F, Zuzow M, Heald N, Gibson A, Shi Y, Goon L, et al. In vitro and in vivo activity of cabozantinib (XL184), an inhibitor of RET, MET, and VEGFR2, in a model of medullary thyroid cancer. Thyroid (2013) 23:1569-77. doi:10.1089/thy.2013.0137.
8. Okamoto K, Kodama K, Takase K, Sugi NH, Yamamoto Y, Iwata M, et al. Antitumor activities of the targeted multi-tyrosine kinase inhibitor lenvatinib (E7080) against RET gene fusion-driven tumor models. Cancer Lett (2013) 340:97-103. doi:10.1016/j.canlet.2013.07.007.
9. Carlomagno F, Anaganti S, Guida T, Salvatore G, Troncone G, Wilhelm SM, et al. Bayer 43-9006 inhibition of oncogenic RET mutants. J Natl Cancer Inst (2006) 98:326-34. doi:10.1093/jnci/djj069.
10. Carlomagno F, Vitagliano D, Guida T, Clardiello F, Tortora G, Vecchio G, et al. ZD6474, an orally available inhibitor of KDR tyrosine kinase activity, efficiently blocks oncogenic RET kinases. Cancer Res (2002) 62:7284-90.
11. Blume-Jensen P, Hunter T. Oncogenic kinase signalling. Nature (2001) 411:355-65. doi:10.1038/35077225.
12. Mitelman F, Johansson B, Mertens F. Fusion genes and rearranged genes as a linear function of chromosome aberrations in cancer. Nat Genet (2004) 36:331-4. doi:10.1038/ng1335.
13. Rikova K, Guo A, Zeng Q, Possemato A, Yu J, Haack H, et al. Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell (2007) 131:1190-203. doi:10.1016/j.cell.2007.11.025.
14. Ou SI, Tan J, Yen Y, Soo RA. ROS1 as a 'druggable' receptor tyrosine kinase: lessons learned from inhibiting the ALK pathway. Expert Rev Anticancer Ther (2012) 12:447-56. doi:10.1586/era.12.17.
15. Charest A, Lane K, McMahon K, Park J, Preisinger E, Conroy H, et al. Fusion of FIG to the receptor tyrosine kinase ROS in a glioblastoma with an interstitial del(6)(q21q21). Genes Chromosomes Cancer (2003) 37:58-71. doi:10.1002/gcc.10207.
16. Lee J, Lee SE, Kang SY, Do I, Lee S, Ha SY, et al. Identification of ROS1 rearrangement in gastric adenocarcinoma. Cancer (2013) 119:1627-35. doi:10.1002/cncr.27967.
17. Aisner DL, Nguyen TT, Paskulin DD, Le AT, Haney J, Schulte N, et al. ROS1 and ALK fusions in colorectal cancer, with evidence of intratumoral heterogeneity for molecular drivers. Mol Cancer Res (2013) 12:111-8. doi:10.1158/1541-7786.MCR-13-0479-T.
18. Takahashi M, Ritz J, Cooper GM. Activation of a novel human transforming gene, ret, by DNA rearrangement. Cell (1985) 42:581-8. doi:10.1016/0092-8674(85)90115-1.
19. Santoro M, Melillo RM, Fusco A. RET/PTC activation in papillary thyroid cancer: European Journal of Endocrinology prize lecture. Eur J Endocrinol (2006) 155:645-53. doi:10.1530/eje.1.02289.
20. Martin-Zanca D, Hughes SH, Barbacid M. A human oncogene formed by the fusion of truncated tropomyosin and protein tyrosine kinase sequences. Nature (1986) 319:741-8. doi:10.1038/319743a0.
21. Longo FM, Massa SM. Small molecule modulation of neurotrophin receptors: a strategy for the treatment of neurological disease. Nat Rev Drug Discov (2013) 12:507-25. doi:10.1038/nrd4024.
22. Greco A, Miranda C, Pierotti MA. Rearrangements of NTRK1 gene in papillary thyroid carcinoma. Mol Cell Endocrinol (2010) 321:44-9. doi:10.1016/j.mce.2009.10.009.
23. O'Bryan JP, Frye RA, Cogswell PC, Neubauer A, Kitch B, Prokop C, et al. axl, a transforming gene isolated from primary human myeloid leukemia cells, encodes a novel receptor tyrosine kinase. Mol Cell Biol (1991) 11:5016-31.
24. Gotlib J, Cools J. Five years since the discovery of PIP1L1-PDGFRA: what we have learned about the fusion and other molecularly defined eosinophilias. Leukemia (2008) 22:1999-2010. doi:10.1038/leu.2008.287.
25. Shaw AT, Hsu PP, Awad MM, Engelman JA. Tyrosine kinase gene rearrangements in epithelial malignancies. Nat Rev Cancer (2013) 11:772-87. doi:10.1038/nrc3612.
26. Shaw AT, Kim DW, Nakagawa K, Seto T, Crinó L, Ahn MJ, et al. Crizotinib versus chemotherapy in advanced ALK-positive lung cancer. N Engl J Med (2013) 368:2385-94. doi:10.1056/NEJMoa1214886.
27. Ou SHI, Bang YJ, Camidge DR, Riely GR, Salgia R, Shapiro G, et al. Efficacy and safety of crizotinib in patients with advanced ROS1-rearranged non-small cell lung cancer (NSCLC). J Clin Oncol (2013) 31(Suppl.):abstr. 8032.
28. Drilon A, Wang L, Hasanovic A, Suehara Y, Lipson D, Stephens P, et al. Response to cabozantinib in patients with RET fusion-positive lung adenocarcinomas. Cancer Discov (2013) 3:630-5. doi:10.1158/2159-8290.CD-13-0035.
29. Ballerini P, Struski S, Cresson C, Prade N, Toujani S, Deswarte C, et al. RET fusion genes are associated with chronic myelomonocytic leukemia and enhance monocytic differentiation. Leukemia (2012) 26:2384-9. doi:10.1038/leu.2012.109.
30. Verma A, Warner SL, Vankayalapati H, Bearss DJ, Sharma S. Targeting Axl and Mer kinases in cancer. Mol Cancer Ther (2011) 10:1763-73. doi:10.1158/1535-7163.MCT-11-0116.
31. Thress K, MacIntyre T, Wang H, Whitston D, Liu ZY, Hoffmann E, et al. Identification and preclinical characterization of AZ-23, a novel, selective, and orally bioavailable inhibitor of the Trk kinase pathway. Mol Cancer Ther (2009) 8:1818-27. doi:10.1158/1535-7163.MCT-09-0036.
32. Weiss GJ, Hidalgo M, Borad MJ, Laheru D, Tibes R, Ramanathan RK, et al. Phase I study of the safety, tolerability and pharmacokinetics of PHA-848125AC, a dual tropomyosin receptor kinase A and cyclin-dependent kinase inhibitor, in patients with advanced solid malignancies. Invest New Drugs (2012) 30:2334-43. doi:10.1007/s10637-011-9774-6.
33. Baccarani M, Cilloni D, Rondoni M, Ottaviani E, Messa F, Merante S, et al. The efficacy of imatinib mesylate in patients with PIP1L1-PDGFRa-positive hypereosinophilic syndrome. Results of a multicenter prospective study. Haematologica (2007) 92:1173-9. doi:10.3324/haematol.11420.
34. Salido M, Pijuan L, Martinez-Aviles L, Galvan AB, Canada I, Rovira A, et al. Increased ALK gene copy number and amplification are frequent in non-small cell lung cancer. J Thorac Oncol (2011) 6:21-7. doi:10.1097/JTO.0b013e3181fb7cd6.
35. Heuckmann JM, Balke-Want H, Malchers F, Peifer M, Sos ML, Koker M, et al. Differential protein stability and ALK inhibitor sensitivity of EML4-ALK fusion variants. Clin Cancer Res (2012) 18:4682-90. doi:10.1158/1078-0432.CCR-11-3260.
36. Paik JJ, Choe G, Kim H, Choe J, Lee JL, Lee C, et al. Screening of anaplastic lymphoma kinase rearrangement by immunohistochemistry in non-small cell lung cancer. Correlation with fluorescence in situ hybridization. J Thorac Oncol (2011) 6:466-72. doi:10.1097/JTO.0b013e31820b82e8.
37. Ying J, Guo L, Qiu T, Shan L, Ling Y, Liu X, et al. Diagnostic value of a novel fully automated immunochemistry assay for detection of ALK rearrangement in primary lung adenocarcinoma. Ann Oncol (2013) 24:2589-93. doi:10.1093/annonc/mdt295.
38. Sholl LM, Sun H, Butaney M, Zhang C, Lee C, Janne PA, et al. ROS1 immunohistochemistry for detection of ROS1-rearranged lung adenocarcinomas. Am J Surg Pathol (2013) 37:1441-9. doi:10.1097/PAS.0b013e3182960fa7.
39. Wang R, Hu H, Pan Y, Li Y, Ye T, Li C, et al. RET fusions define a unique molecular and clinicopathologic subtype of non-small-cell lung cancer. J Clin Oncol (2012) 30:4352-9. doi:10.1200/JCO.2012.44.1477.
40. Li T, Maus MKH, Desai SJ, Beckett LA, Stephens C, Huang E, et al. Large-scale screening and molecular characterization of EML4-ALK fusion variants in archival non-small-cell lung cancer tumor specimens using quantitative reverse transcription polymerase chain reaction assays. J Thorac Oncol (2014) 9:18-25. doi:10.1097/JTO.0000000000000030.
41. Peled N, Palmer G, Hirsch FR, Wynes MW, Ilouze M, Varella-Garcia M, et al. Next-generation sequencing identifies and immunohistochemistry confirms a novel crizotinib-sensitive ALK rearrangement in a patient with metastatic non-small-cell lung cancer. J Thorac Oncol (2012) 7:e14-6. doi:10.1097/JTO.0b013e3182614ab5.
42. Fridlyand J, Simon RM, Walrath JC, Roach N, Buller R, Schenkein DP, et al. Considerations for the successful co-development of targeted cancer therapies and companion diagnostics. Nat Rev Drug Discov (2013) 10:743-55. doi:10.1038/nrd4101.