Next-generation sequencing of stage IV squamous cell lung cancers reveals an association of PI3K aberrations and evidence of clonal heterogeneity in patients with brain metastases

Cancer Discovery

Volumn 5, Issue 6, 2016, Pages 610-621

  Paik, Paul K ^a,b   Shen, Ronglai ^a   Won, Helen ^a   Rekhtman, Natasha ^a   Wang, Lu ^a   Sima, Camelia S ^a   Arora, Arshi ^a   Seshan, Venkatraman ^a   Ladanyi, Marc ^a   Berger, Michael F ^a,b   Kris, Mark G ^a,b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR 1; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; SERINE PROTEINASE INHIBITOR;

ADULT; AGE; AGED; ARTICLE; BRAIN METASTASIS; CHROMOSOME ABERRATION; DISEASE SEVERITY; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENDER; GENE MUTATION; GENE OVEREXPRESSION; GENETIC HETEROGENEITY; GENOTYPE; HUMAN; KARNOFSKY PERFORMANCE STATUS; MAJOR CLINICAL STUDY; MALE; NEXT GENERATION SEQUENCING; OVERALL SURVIVAL; SMOKING; SQUAMOUS CELL LUNG CARCINOMA; WNT SIGNALING PATHWAY; BRAIN TUMOR; CANCER STAGING; CARCINOMA, SQUAMOUS CELL; CLONAL EVOLUTION; COPY NUMBER VARIATION; DEFICIENCY; DNA MUTATIONAL ANALYSIS; GENE AMPLIFICATION; GENE EXPRESSION; GENETIC VARIATION; GENETICS; HIGH THROUGHPUT SEQUENCING; KAPLAN MEIER METHOD; LUNG NEOPLASMS; METABOLISM; METASTASIS; MIDDLE AGED; MORTALITY; MUTATION; PATHOLOGY; RISK FACTOR; SECONDARY; SIGNAL TRANSDUCTION; VERY ELDERLY;

AGED; AGED, 80 AND OVER; BRAIN NEOPLASMS; CARCINOMA, SQUAMOUS CELL; CLONAL EVOLUTION; DNA COPY NUMBER VARIATIONS; DNA MUTATIONAL ANALYSIS; FEMALE; GENE AMPLIFICATION; GENE EXPRESSION; GENETIC VARIATION; GENOTYPE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; KAPLAN-MEIER ESTIMATE; LUNG NEOPLASMS; MALE; MIDDLE AGED; MUTATION; NEOPLASM METASTASIS; NEOPLASM STAGING; PHOSPHATIDYLINOSITOL 3-KINASES; PTEN PHOSPHOHYDROLASE; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; RISK FACTORS; SERPINS; SIGNAL TRANSDUCTION;

EID: 84980047658     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-14-1129     Document Type: Article

References (41)

1. Elliott J, Ahmedzai S, Hole D, Dorward A, Stevenson R, Kaye S, et al. Vindesine and cisplatin combination chemotherapy compared with vindesine as a single agent in the management of non-small cell lung cancer: a randomized study. Eur J Cancer Clin Oncol 1984; 20: 1025–32.
2. Rekhtman N, Paik P, Arcila M, Tafe L, Oxnard G, Moreira A, et al. Clarifying the spectrum of driver oncogene mutations in pure, biomarkerverified squamous carcinoma of lung: lack of EGFR/KRAS and presence of PIK3CA/AKT1 mutations. Clin Cancer Res 2011; 18: 1167–76.
3. The Cancer Genome Atlas. Comprehensive genomic characterization of squamous cell lung cancers. Nature 2012; 489: 519–25.
4. Weiss J, Sos ML, Seidel D, Peifer M, Zander T, Heuckmann JM, et al. Frequent and focal FGFR1 amplification associates with therapeutically tractable FGFR1 dependency in squamous cell lung cancer. Sci Transl Med 2010; 2: 62–93.
5. Hammerman PS, Sos ML, Ramos AH, Xu C, Dutt A, Zhou W, et al. Mutations in the DDR2 kinase gene identify a novel therapeutic target in squamous cell lung cancer. Cancer Discov 2011; 1: 78–89.
6. Xu C, Fillmore Christine M, Koyama S, Wu H, Zhao Y, Chen Z, et al. Loss of Lkb1 and Pten leads to lung squamous cell carcinoma with elevated PD-L1 expression. Cancer Cell 2014; 25: 590–604.
7. Spoerke JM, O’Brien C, Huw L, Koeppen H, Fridlyand J, Brachmann RK, et al. Phosphoinositide 3-Kinase (PI3K) pathway alterations are associated with histologic subtypes and are predictive of sensitivity to PI3K inhibitors in lung cancer preclinical models. Clin Cancer Res 2012; 18: 6771–83.
8. Drilon A, Rekhtman N, Ladanyi M, Paik P. Squamous-cell carcinomas of the lung: emerging biology, controversies, and the promise of targeted therapy. Lancet Oncol 2012; 13: e418–e26.
9. Saal LH, Johansson P, Holm K, Gruvberger-Saal SK, She Q-B, Maurer M, et al. Poor prognosis in carcinoma is associated with a gene expression signature of aberrant PTEN tumor suppressor pathway activity. Proc Natl Acad Sci 2007; 104: 7564–9.
10. Nguyen DX, Chiang AC, Zhang XHF, Kim JY, Kris MG, Ladanyi M, et al. WNT/TCF signaling through LEF1 and HOXB9 mediates lung adenocarcinoma metastasis. Cell 2009; 138: 51–62.
11. Valiente M, Obenauf Anna C, Jin X, Chen Q, Zhang Xiang HF, Lee Derek J, et al. Serpins promote cancer cell survival and vascular co-option in brain metastasis. Cell 2014; 156: 1002–16.
12. Soria J-C, Lee H-Y, Lee JI, Wang L, Issa J-P, Kemp BL, et al. Lack of PTEN expression in non-small cell lung cancer could be related to promoter methylation. Clin Cancer Res 2002; 8: 1178–84.
13. Craddock KJ, Ludkovski O, Sykes J, Shepherd FA, Tsao M-S. Prognostic value of fibroblast growth factor receptor 1 gene locus amplification in resected lung squamous cell carcinoma. J Thorac Oncol 2013; 8: 1371–7.
14. Kim HR, Kim DJ, Kang DR, Lee JG, Lim SM, Lee CY, et al. Fibroblast growth factor receptor 1 gene amplification is associated with poor survival and cigarette smoking dosage in patients with resected squamous cell lung cancer. J Clin Oncol 2013; 31: 731–7.
15. Tran TN, Selinger CI, Kohonen-Corish MRJ, McCaughan BC, Kennedy CW, O’Toole SA, et al. Fibroblast growth factor receptor 1 (FGFR1) copy number is an independent prognostic factor in nonsmall cell lung cancer. Lung Cancer 2013; 81: 462–7.
16. Russell PA, Yu Y, Young RJ, Conron M, Wainer Z, Alam N, et al. Prevalence, morphology, and natural history of FGFR1-amplified lung cancer, including squamous cell carcinoma, detected by FISH and SISH. Mod Pathol 2014; 27: 1621–31.
17. Zhang J, Zhang L, Su X, Li M, Xie L, Malchers F, et al. Translating the therapeutic potential of AZD4547 in FGFR1-amplified non–small cell lung cancer through the use of patient-derived tumor xenograft models. Clin Cancer Res 2012; 18: 6658–67.
18. Paik P, Shen R, Ferry D, Soria J-C, Mathewson A, Kilgour E, et al. A phase 1b open-label multicenter study of AZD4547 in patients with advanced squamous cell lung cancers: Preliminary antitumor activity and pharmacodynamic data. J Clin Oncol 2014; 32: suppl; abstr 8035.
19. Nogova L, Sequist L, Cassier P, Hidalgo M, Delord J-P, Schuler M, et al. Targeting FGFR1-amplified lung squamous cell carcinoma with the selective pan-FGFR inhibitor BGJ398. J Clin Oncol 2014; 32: suppl; abstr 8034.
20. Wynes MW, Hinz TK, Gao D, Martini M, Marek LA, Ware KE, et al. FGFR1 mRNA and protein expression, not gene copy number, predict FGFR TKI sensitivity across all lung cancer histologies. Clin Cancer Res 2014; 20: 3299–309.
21. Stenbygaard LE, Sorensen JB, Olsen JE. Metastatic pattern in adenocarcinoma of the lung: an autopsy study from a cohort of 137 consecutive patients with complete resection. J Thorac Cardiovasc Surg 1995; 110: 1130–5.
22. Niessner H, Forschner A, Klumpp B, Honegger JB, Witte M, Bornemann A, et al. Targeting hyperactivation of the AKT survival pathway to overcome therapy resistance of melanoma brain metastases. Cancer Med 2013; 2: 76–85.
23. A damo B, Deal A, Burrows E, Geradts J, Hamilton E, Blackwell K, et al. Phosphatidylinositol 3-kinase pathway activation in breast cancer brain metastases. Breast Cancer Res 2011; 13: R125.
24. Li Q, Yang J, Yu Q, Wu H, Liu B, Xiong H, et al. Associations between single-nucleotide polymorphisms in the PI3K–PTEN–AKT–mTOR pathway and increased risk of brain metastasis in patients with non–small cell lung cancer. Clin Cancer Res 2013; 19: 6252–60.
25. Tamura M, Gu J, Matsumoto K, Aota S-i, Parsons R, Yamada KM. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science 1998; 280: 1614–7.
26. Frank M, Ebert M, Shan W, Phillips GR, Arndt K, Colman DR, et al. Differential expression of individual gamma-protocadherins during mouse brain development. Mol Cell Neurosci 2005; 29: 603–16.
27. Zhang J, Fujimoto J, Zhang J, Wedge DC, Song X, Zhang J, et al. Intratumor heterogeneity in localized lung adenocarcinomas delineated by multiregion sequencing. Science 2014; 346: 256–9.
28. de Bruin EC, McGranahan N, Mitter R, Salm M, Wedge DC, Yates L, et al. Spatial and temporal diversity in genomic instability processes defines lung cancer evolution. Science 2014; 346: 251–6.
29. Rekhtman N, Ang D, Sima C, Travis W, Moreira A. Immunohistochemistry algorithm for differentiation of lung adenocarcinoma and squamous cell carcinoma based on a large series of whole-tissue sections with validation in small specimens. Mod Pathol 2011; 24: 1348–59.
30. Won H, Scott S, Brannon A, Shah R, Berger M. Detecting somatic genetic alterations in tumor specimens by exon capture and massively parallel sequencing. J Vis Exp 2013; 80: e50710.
31. Cheng D, Mitchell T, Zehir A, Shah R, Benayed R, Syed A, et al. Memorial Sloan Kettering-Integrated Mutation Profiling of Actionable Cancer Targets (MSK-IMPACT): a hybridization capture-based next-generation sequencing clinical assay for solid tumor molecular oncology. J Mol Diagn 2015;17:251–64.
32. Wagle N, Berger MF, Davis MJ, Blumenstiel B, DeFelice M, Pochanard P, et al. High-throughput detection of actionable genomic alterations in clinical tumor samples by targeted, massively parallel sequencing. Cancer Discov 2012; 2: 82–93.
33. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009; 25: 1754–60.
34. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20: 1297–303.
35. Cibulskis K, Lawrence MS, Carter SL, Sivachenko A, Jaffe D, Sougnez C, et al. Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat Biotech 2013; 31: 213–9.
36. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 2011; 39: D945–D50.
37. Institute B. Picard. 2015. Available from: http://broadinstitute.github.io/picard/
38. Ramos AH, Lichtenstein L, Gupta M, Lawrence MS, Pugh TJ, Saksena G, et al. Oncotator: cancer variant annotation tool. Hum Mutat 2015; 36: E2423–9.
39. Seshan V. Detecting copy number changes and structural rearrangements using DNA sequencing. In: Datta S, Nettleton D, editors. Statistical Analysis of Next Generation Sequencing Data. Switzerland: Springer; 2014. p. 355–78.
40. Shen R, Seshan V. FACETS: fraction and allele-specific copy number estimates from tumor sequencing Memorial Sloan-Kettering Cancer Center, Dept of Epidemiology & Biostatistics Working Paper Series. 2015: Working Paper 29.
41. Roth A, Khattra J, Yap D, Wan A, Laks E, Biele J, et al. PyClone: statistical inference of clonal population structure in cancer. Nat Methods 2014; 11: 396–8.